Readings

Introduction to the Visual System. Organization of the Retina.

Major Topics: Anatomy and Physiology of the Retina, Ganglion-cell Receptive Field Organization, Pre-ganglionic Elements.

Assigned Readings:

Background: Schiller, Peter H. "The Central Visual System." Vision Research 26 (1986): 1351-1355. (Read sections on retina.)

Werblin, F. W., and J. E. Dowling. "Organization of the Retina of the Mudpuppy, Necturus maculosus. II. Intracellular Recording." J. Neurophysiol. 32 (1969): 339-355.

Wassle, H., and B. B. Boycott. "Functional Architecture of the Mammalian Retina." Physiological Reviews 71 (1991): 447-480.

Dacey, Dennis M. "The Mosaic of Midget Ganglion Cells in the Human Retina." J. Neurosci. 13 (1993): 5334-5355.

PubMed abstract:  To study their detailed morphology, ganglion cells of the human retina were stained by intracellular tracer injection, in an in vitro, whole-mount preparation. This report focuses on the dendritic morphology and mosaic organization of the major, presumed color-opponent, ganglion cell class, the midget cells. Midget cells in the central retina were recognized by their extremely small dendritic trees, approximately 5-10 microns in diameter. Between 2 and 6 mm eccentricity, midget cells showed a steep, 10-fold increase in dendritic field size, followed by a more shallow, three- to fourfold increase in the retinal periphery, attaining a maximum diameter of approximately 225 microns. Despite large local variation in dendritic field size, midget cells formed one morphologically distinctive class at all retinal eccentricities. Two midget cell types were distinguished by their dendritic stratification in either the inner or outer portion of the inner plexiform layer (IPL), and presumably correspond to ON- and OFF-center cells respectively. The mosaic organization of the midget cells was examined by intracellularly filling neighboring cells in small patches of retina. For both the inner and outer midget populations, adjacent dendritic trees apposed one another but did not overlap, establishing a coverage of no greater than 1. The two mosaics differed in spatial scale, however: the outer midget cells showed smaller dendritic fields and higher cell density than the inner midget cells. An outer:inner cell density ratio of 1.7:1 was found in the retinal periphery. An estimate of total midget cell density suggested that the proportion of midget cells increases from about 45% of total ganglion cell density in the retinal periphery to about 95% in the central retina. Nyquist frequencies calculated from midget cell spacing closely match a recent measure of human achromatic spatial acuity (Anderson et al., 1991), from approximately 6 degrees to 55 degrees eccentricity. Outside the central retina, midget cell dendrites arborized in clusters within the overall dendritic field. With increasing eccentricity, the dendritic clusters increased in number and remained small (approximately 10-20 microns diameter) relative to the size of the dendritic field. Because neighboring midget cell dendritic trees do not overlap, the mosaic as a whole showed a pattern of clusters and holes. We hypothesize that midget cell dendritic trees may contact individual axon terminals of some midget bipolar cells and avoid contacting others, providing a basis for the formation of cone-specific connections in the IPL.

Assigned Readings:

Schiller, P. H., and J. G. Malpeli. "Functional Specificity of Lateral Geniculate Nucleus Laminae of the Rhesus Monkey." J. Neurophysiol. 41 (1978): 788-797.

PubMed abstract:  This study investigated the functional specificity of the lateral geniculate mucleus (LGN) of the rhesus monkey using microelectrode-recording techniques. 2. The parvocellular laminae of the LGN receive input predominantly from medium-conduction-velocity optic tract fibers, while the magnocellular laminae receive fast-conducting axons from the retina. 3. Cells projecting from the parvocellular layers to area 17 have medium-conduction velocities, while those from the magnocellular layers are fast conducting. 4. The majority of cells in the parvocellular layers have a concentric color-opponent receptive-field organization. The receptive fields of magnocellular layers cells are also concentrically organized, but their center-surround organization is independent of wavelength. 5. Responses in the parvocellular layers are more sustained than in the magnocellular layers. 6. Cells in the dorsal pair of parvocellular layers are predominantly on-center. In the ventral pair of parvocellular layers, most cells are off-center. 7. Blue-selective cells are found predominantly in the ventral pair of parvocellular layers. All of these found gave on-responses to blue stimuli.

Hendry, S. H. C., and T. Y. Yoshioka. "A Neurochemically Distinct Third Channel in the Macaque Dorsal Lateral Geniculate Nucleus." Science 264 (1994): 575-577.

PubMed abstract:  The primate visual system is often divided into two channels, designated M and P, whose signals are relayed to the cerebral cortex by neurons in the magnocellular and parvicellular layers of the dorsal lateral geniculate nucleus. We have identified a third population of geniculocortical neurons in the dorsal lateral geniculate nucleus of macaques, which is immunoreactive for the alpha subunit of type II calmodulin-dependent protein kinase. This large third population occupies interlaminar regions (intercalated layers) ventral to each principal layer. Retrograde labeling of kinase-immunoreactive cells from the primary visual cortex shows that they provide the geniculocortical input to cytochrome oxidase-rich puffs in layers II and III.

Assigned Readings:

Background: Schiller, P. H. "The Central Visual System." Vision Research 26 (1986): 1357-1363. (Read sections on the striate cortex.)

Hubel, D., and T. N. Wiesel. "Receptive Fields, Binocular Interaction and Functional Architecutre in the Cat's Visual Cortex." J. Physiol. 160 (1962): 106-154.

Leventhal, A. G., K. G. Thompson, D. Liu, Y. Zhou, and S. J. Ault. "Concomitant Sensitivity to Orientation, Direction and Color of Cells in Layers 2,3, and 4 of Monkey Striate Cortex." J. Neurosci. 15 (1995): 1808-1818.

PubMed abstract:  The receptive field properties of cells in layers 2, 3, and 4 of area 17 (V1) of the monkey were studied quantitatively using colored and broad-band gratings, bars, and spots. Many cells in all regions studied responded selectively to stimulus orientation, direction, and color. Nearly all cells (95%) in layers 2 and 3 exhibited statistically significant orientation preferences (biases), most exhibited at least some color sensitivity, and many were direction sensitive. The degree of selectivity of cells in layers 2 and 3 varied continuously among cells; we did not find discrete regions containing cells sensitive to orientation and direction but not color, and vice versa. There was no relationship between the degree of orientation sensitivity of the cells studied and their degree of color sensitivity. There was also no obvious relationship between the receptive field properties studied and the cells' location relative to cytochrome oxidase-rich regions. Our findings are difficult to reconcile with the hypothesis that there is a strict segregation of cells sensitive to orientation, direction, and color in layers 2 and 3. In fact, the present results suggest the opposite since most cells in these layers are selective for a number of stimulus attributes.

Recommended Readings:

Hubel, D. H., and T. N. Wiesel. "Receptive Fields and Functional Architecture of Monkey Striate Cortex." J. Physiol. 195, London (1968): 215-243.

Blasdel, G. G. "Orientation Selectivity, Preference, and Continuity in Monkey Striate Cortex." J. Neurosci. 12 (1992): 3139-3161.

PubMed abstract:  Maps of orientation preference and selectivity, inferred from differential images of orientation (Blasdel, 1992), reveal linear organizations in patches, 0.5-1.0 mm across, where orientation selectivities are high, and where preferred orientations rotate linearly along one axis while remaining constant along the other. Most of these linear zones lie between the centers of adjacent ocular dominance columns, with their short iso-orientation slabs oriented perpendicular, in regions enjoying the greatest binocular overlap. These two-dimensional linear zones are segregated by one- and zero-dimensional discontinuities that are particularly abundant in the centers of ocular dominance columns, and that are also correlated with cytochrome oxidase-rich zones within them. Discontinuities smaller than 90 degrees extend in one dimension, as fractures, while discontinuities greater than 90 degrees are confined to points, in the form of singularities, that are generated when orientation preferences rotate continuously through +/- 180 degrees along circular paths. The continuous rotations through 180 degrees imply that direction preferences are not organized laterally in striate cortex. And they also ensure that preferences for all orientations converge at each singularity, with perpendicular orientations represented uniquely close together on opposite sides. The periodic interspersing of linear zones and singularities suggests that orientation preferences are organized by at least two competing schemes. They are optimized for linearity, along with selectivity and binocularity, in the linear zones, and they are optimized for density near singularities. Since upper-layer neurons are likely to have similarly sized dendritic fields in all regions (Lund and Yoshioka, 1991), those in the linear zones should receive precise information about narrowly constrained orientations, while those near singularities should receive coarse information about all orientations--very different inputs that suggest different perceptual functions.

Blasdel, G. G. "Differential Imaging of Ocular Dominance and Orientation Selectivity in Monkey Striate Cortex." J. Neurosci. 12 (1992): 3115-3138.

PubMed abstract:  Differential images of ocular dominance, acquired by comparing responses to the two eyes, reveal dark and light bands where cortical cells are dominated by the right and left eyes. These include most (but not all) histochemically stained cytochrome oxidase blobs in their centers. Differential images of orientation, acquired by comparing responses to orthogonal orientations, reveal dark and light bands that are reminiscent of the "orientation columns" reported earlier, on the basis of 2-deoxyglucose (2DG) autoradiograms (Hubel et al., 1978). However, they are shorter and more fragmented because they do not include regions lacking selectivity for orientation. Even though these "bands" derive from orientation-selective areas, comparisons with differential images of other orientations reveal that regions along their centers prefer different orientations. Hence, the orientation preferences inferred from "bands" in single differential images, or single 2DG autoradiograms, are not necessarily incorrect. Interactions between ocular dominance and orientation were investigated by comparing differential images of orientation obtained with binocular and monocular stimulation, as well as by comparing differential images of ocular dominance obtained with different orientations. In both cases, the elicited interactions were minimal, indicating a remarkable and unexpected independence that subsequent experiments revealed arises, at least in part, from a lateral segregation of regions most selective for one eye and regions most selective for one orientation, in the centers and edges of ocular dominance columns. Since this can also be viewed as a lateral correlation between binocularity and orientation selectivity, it fits with the simultaneous emergence of these properties in layers receiving input from layer 4c, and suggests that each of these properties requires the other.

Frostig, R. D. "What Does in Vivo Optical Imaging Tell Us About the Primary Visual Cortex in Primates?" In Cerebral Cortex. Vol. 10. Edited by A. Peters, and K. S. Rockland. New York: Plenum Press, 1994.

Peters, A. "The Organization of the Primary Visual Cortex in the Macaque." In Cerebral Cortex. Vol. 10. Edited by A. Peters, and K. S. Rockland, New York: Plenum Press, 1994.

Schiller, P. H., B. L. Finlay, and S. F. Volman. "Quantitative Studies of Single-cell Properties in Monkey Striate Cortex I, II and III." J. Neurophysiol. 39 (1976): 1288-1351.

PubMed abstract:  The properties of single cells in striate cortex of the rhesus monkey, representing the visual field 2 degrees -5 degrees from the fovea, were examined quantitatively with stationary and moving stimuli. Three distinct classes of cells were identified: S type, CX type, and T type. 2. S-type cells were defined as those oriented cells which to the optimal direction of movement in their receptive fields exhibited one or more spatially separate subfields within each of which a response was obtained to either a light or dark edge, but not to both. Several different types of S-cells were distinguished: a) S1-type cells for which moving edges revealed a single excitatory area within which a response was elicited by either a light or a dark edge but not by both. Most of these cells were unidirectional. b) S2-type cells for which moving edges revealed two spatially separate response areas, one of which was excited by a light edge and the other by a dark edge. Both regions responded to the same direction of movement. c) S3-type cells which had two response areas, one of which was excited by a stimulus moving in one direction (at right angles to the axis of orientation) and the other, of opposite contrast, which responded in the opposite direction, d) S4-type cells which to one direction of movement showed two spatially separate regions sensitive to a light and dark edge and which in the other direction of movement had only one responsive area (either light or dark). e) Cells which had multiple spatially separate subfields (S5-7 types). 3. CX-type cells were defined as those oriented cells which in their receptive fields exhibited no spatial separation for light- and dark-edge responses; they discharged to both edges in the same direction of movement and in the same spatial area. Flashing stimuli elicited both on and off responses throughout the receptive field. CX-type cells were predominantly of two types: those which were selective for direction of stimulus movement and those which were not. 4. A third class of cells (T-type) were those which were excited by only one sign of contrast change and responded in a sustained fashion even when there was no contour within the receptive field. These cells were poorly or not at all oriented; some of them were selective to wavelength. 5. Quantitative comparisons showed the following differences between S-type and CX-type cells: a) S-type cells had smaller receptive fields than CX-type cells but the populations over-lapped considerably. Receptive-field size was smallest in layer 4c. In all other layers S-type cells had the same size fields. CX-type cells, by contrast, tended to have larger fields in layer 5-6 than 2-3. b) The spatial separation between light and dark response areas was the best criterion for distinguishing S-type and CX-type cells. The distribution of this measure disclosed two populations of cells with relatively limited overlap. c) In layers 2 and 3, both S-type and CX-type cells had low spontaneous activity.

Research Reports:

Roorda, A., and D. R. Williams. "The Arrangement of the Three Cone Classes in the Living Human Eye." Nature 397 (1999): 520-522.

PubMed abstract:  Human colour vision depends on three classes of receptor, the short- (S), medium- (M), and long- (L) wavelength-sensitive cones. These cone classes are interleaved in a single mosaic so that, at each point in the retina, only a single class of cone samples the retinal image. As a consequence, observers with normal trichromatic colour vision are necessarily colour blind on a local spatial scale. The limits this places on vision depend on the relative numbers and arrangement of cones. Although the topography of human S cones is known, the human L- and M-cone submosaics have resisted analysis. Adaptive optics, a technique used to overcome blur in ground-based telescopes, can also overcome blur in the eye, allowing the sharpest images ever taken of the living retina. Here we combine adaptive optics and retinal densitometry to obtain what are, to our knowledge, the first images of the arrangement of S, M and L cones in the living human eye. The proportion of L to M cones is strikingly different in two male subjects, each of whom has normal colour vision. The mosaics of both subjects have large patches in which either M or L cones are missing. This arrangement reduces the eye's ability to recover colour variations of high spatial frequency in the environment but may improve the recovery of luminance variations of high spatial frequency.

Nirenberg, S., S. M. Carciery, A. L. Jacobs, and P. E. Latham. "Retinal Ganglion Cells Act Largely as Independent Encoders." Nature 411 (2001): 698-700.

PubMed abstract:  Correlated firing among neurons is widespread in the visual system. Neighbouring neurons, in areas from retina to cortex, tend to fire together more often than would be expected by chance. The importance of this correlated firing for encoding visual information is unclear and controversial. Here we examine its importance in the retina. We present the retina with natural stimuli and record the responses of its output cells, the ganglion cells. We then use information theoretic techniques to measure the amount of information about the stimuli that can be obtained from the cells under two conditions: when their correlated firing is taken into account, and when their correlated firing is ignored. We find that more than 90% of the information about the stimuli can be obtained from the cells when their correlated firing is ignored. This indicates that ganglion cells act largely independently to encode information, which greatly simplifies the problem of decoding their activity.

Zrenner, E. "Will Retinal Implants Restore Vision?" Science 295 (2002): 1022-1025.

PubMed abstract:  A number of research groups are developing electrical implants that can be attached directly to the retina in an attempt to restore vision to patients suffering from retinal degeneration. However, despite promising results in animal experiments, there are still several major obstacles to overcome before retinal prostheses can be used clinically.

Assigned Readings:

Background: Schiller, P. H. "The Central Visual System." Vision Research 26 (1986): 1363-1372. (Read sections on higher cortical areas.)

Kaas, J. H., and D. C. Lyon. "Visual Cortex Organization in Primates: Theories of V3 and Adjoining Visual Areas." Chap. 18 in Vision: from Neurons to Cognition. Edited by C. Casanova, and M. Ptito. Progress in Brain Research. Vol. 134. Amsterdam, Elsevier, 2001.

PubMed abstract:  After years of experimentation and substantial progress, there is still only limited agreement on how visual cortex in primates is organized, and what features of this organization are variable or stable across lines of primate phylogeny. Only three visual areas, V1, V2, and MT, are widely recognized as common to all primates, although there are certainly more. Here we consider various concepts of how the cortex along the outer border of V2 is organized. An early proposal was that this region is occupied by a V3 that is as wide and as long as V2, and represents the visual hemifield as a mirror image of V2. We refer to this notion as the classical V3 or V3-C. Another proposal is that only the dorsal half of V3-C exists, the half representing the lower visual quadrant, and thus the representation is incomplete (V3-I) by half. A version of this proposal is that V3-I is discontinuous, extremely thin in places, and highly variable across individuals, much as a vestigial or degenerate structure might be (V3-IF-incomplete and fragmented). A fourth proposal is that there is no V3. Many results suggest that a series of visual areas border V2, none of which has the characteristics of V3. Alternatively, the possibility exists that primate taxa differ with regard to visual areas bordering V2. Currently, much of the supporting evidence for a classical V3 comes from fMRI studies in humans, much of the evidence for a series of bordering areas comes from New World Monkeys and prosimian galagos, and much of the evidence for a V3-I or V3-IF comes from macaque monkeys. Possibly all these interpretations of visual cortex organization are valid, but each for only one of the major groups of primate evolution. Here, we suggest that none of these interpretations is correct, and propose instead that a modified V3 (V3-M) exists in a similar form in all primates. This V3-M is smaller and thinner than V3-C, discontinuous in the middle, but with comparable dorsal and ventral halves representing the lower and upper visual hemifields, respectively. Because the evidence for V3-M is limited, and it stems in part from our ongoing but incomplete comparative studies of V1 connections in primates, this suggestion requires further experimental evaluation and it remains tentative.

Levitt, J. B., D. C. Kiper, and J. A. Movshon. "Receptive Fields and Functional Architecture of Macaque V2." Journal of Neurophysiol. 71 (1994): 2517-2542.

PubMed abstract:  Visual area V2 of macaque monkey cerebral cortex is the largest of the extrastriate visual areas, yet surprisingly little is known of its neuronal properties. We have made a quantitative analysis of V2 receptive field properties. Our set of measurements was chosen to distinguish neuronal responses reflecting parvocellular (P) or magnocellular (M) inputs and to permit comparison with similar measurements made in other visual areas; we further describe the relationship of those properties to the laminar and cytochrome oxidase (CO) architecture of V2. 2. We recorded the activity of single units representing the central 5 degrees in all laminae and CO divisions of V2 in anesthetized, paralyzed macaque monkeys. We studied responses to geometric targets and to drifting sinusoidal gratings that varied in orientation, spatial frequency, drift rate, contrast, and color. 3. The orientation selectivity and spatial and temporal tuning of V2 neurons differed little from those in V1. As in V1, spatial and temporal tuning in V2 appeared separable, and we identified a population of simple cells (more common within the central 3 degrees) similar to those found in V1. Contrast sensitivity of V2 neurons was greater on average than in V1, perhaps reflecting the summation of inputs in V2's larger receptive fields. Many V2 neurons exhibited some degree of chromatic opponency, responding to isoluminant color variations, but these neurons differed from V1 in the linearity with which they summate cone signals. 4. In agreement with others, we found that neurons with selective responses to color, size, and motion did seem to cluster in different CO compartments. However, this segregation of qualitatively different response selectivities was not absolute, and response properties also seemed to depend on laminar position within each compartment. As others also have noted, we found that CO stripe widths in the macaque (unlike in the squirrel monkey) did not consistently appear different. We relied on the segregation of qualitatively distinct cell types, and in some cases the pattern of Cat-301 staining as well, to distinguish CO stripes when the staining pattern of CO alone was ambiguous. Although all cell types were found in all CO compartments and laminae, unoriented cells were more prominent in layers 2-4 of "thin" stripes, direction-selective cells in layers 3B/4 of "thick" stripes, color-selective cells in the upper layers of thin and pale stripes, and end-stopped cells mainly outside of layer 4 in thin stripes.

Maunsell, J. H. R., and D. C. VanEssen. "Functional Properties of Neurons in Middle Temporal Visual Area of the Macaque Monkey I and II." J. Neurophysiol. 49 (1983): 1127-1167.

PubMed abstract:  Recordings were made from single units in the middle temporal visual area (MT) of anesthetized, paralyzed macaque monkeys. A computer-driven stimulator was used to make quantitative tests of selectivity for stimulus direction, speed, and orientation. The data were taken from 168 units that were histologically identified as being in MT. 2. The results confirm previous reports of a high degree of direction selectivity in MT. The response above background to stimuli moving in a unit's preferred direction was, an average, 10.9 times that to stimuli moving in the opposite direction. There was a marked tendency for nearby units to have similar preferred directions. 3. Most units were also sharply tuned for the speed of stimulus motion. For some cells the response fell to less than half-maximal at speeds only a factor of two from the optimum; on average, responses were greater than half-maximal only over a 7.7-fold range of speed. The distribution of preferred speeds for different units was unimodal, with a peak near 32 degrees/s; the total range of preferred speeds extended from 2 to 256 degrees/s. Nearby units generally responded best to similar speeds of motion. 4. Most units in MT showed selectivity for stimulus orientation when tested with stationary, flashed bars. However, stationary stimuli generally elicited only brief responses; when averaged over the duration of the stimulus, the responses were much less than those to moving stimuli. The preferred orientation was usually, but not always, perpendicular to the preferred direction of movement. 5. A comparison of the results of the present study with a previous quantitative investigation in the owl monkey shows a striking similarity in response properties in MT of the two species. 6. The presence of both direction and speed selectivity in MT of the macaque suggests that this area is more specialized for the analysis of visual motion than has been previously recognized.

Recommended Readings:

Gross, C. G. "From Imhotep to Hubel and Wiesel: The Story of Visual Cortex." In Cerebral Cortex. Edited by Rockland, Kaas, and Peters. Plenum Press, 1997.

Kaas, J. H. "Theories of Visual Cortex Organization in Primates." In Cerebral Cortex. Edited by Rockland, Kaas, and Peters. Plenum Press, 1997.

Research Reports:

Sereno, M. I., et al. "Borders of Multiple Visual Areas in Humans Revealed by Functional Magnetic Resonance Imaging." Science 268 (1995): 889-893.

PubMed abstract:  The borders of human visual areas V1, V2, VP, V3, and V4 were precisely and noninvasively determined. Functional magnetic resonance images were recorded during phase-encoded retinal stimulation. This volume data set was then sampled with a cortical surface reconstruction, making it possible to calculate the local visual field sign (mirror image versus non-mirror image representation). This method automatically and objectively outlines area borders because adjacent areas often have the opposite field sign. Cortical magnification factor curves for striate and extrastriate cortical areas were determined, which showed that human visual areas have a greater emphasis on the center-of-gaze than their counterparts in monkeys. Retinotopically organized visual areas in humans extend anteriorly to overlap several areas previously shown to be activated by written words.

DeYoe, E. A., D. J. Felleman, D. C. Van Essen, and E. McClendon. "Multiple Processing Streams in Occipitotemporal Visual Cortex." Nature 371 (1994): 151-154.

The earliest stages of cortical visual processing in areas V1 and V2 of the macaque monkey contain internal subdivisions ('blobs' and 'interblobs' in layer 4B in V1; thin, thick and interstripes in V2) that are selectively interconnected and contain neurons with distinctive visual response properties. Here we use anatomical pathway tracing to demonstrate that higher visual areas, V4 and the ventral posterior inferotemporal cortex, each contain anatomical subdivisions that have distinct input and output projections. These findings, in conjunction with others, suggest that modularity and multistream processing within individual cortical areas are widespread features of neocortical organization.

Murphy, P. C., S. G. Duckett, and A. M. Sillito. "Feedback Connections to the Lateral Geniculate Nucleus and Cortical Reponse Properties." Science 286 (1999): 1552-1554.

PubMed abstract:  The cerebral cortex receives sensory input from the periphery by means of thalamic relay nuclei, but the flow of information goes both ways. Each cortical area sends a reciprocal projection back to the thalamus. In the visual system, the synaptic relations that govern the influence of thalamic afferents on orientation selectivity in the cortex have been studied extensively. It now appears that the connectivity of the corticofugal feedback pathway is also fundamentally linked to the orientation preference of the cortical cells involved.

Assigned Readings:

Hartline, H. K. "The Responses of Single Optic Nerve Fibers of the Vertebrate Eye to Illumination of the Retina." Am. J. Physiol 121 (1938): 400-415.

Kuffler, S. W. "Discharge Patterns and Functional Organization of Mammalian Retina." J. Neurophysiol 16 (1953): 37-68.

Schiller, P. H. "The ON and OFF Channels of the Mammalian Visual System." Progress in Retinal and Eye Research 15 (1995).

Schiller, P. H. "The Central Connections of the Retinal ON and OFF Pathways." Nature 297 (1982): 580-583.

Schiller, P. H., J. H. Sandell, and J. H. R. Maunsell. "The functions of the ON and OFF channels of the visual system." Nature 322 (1986): 824-825.

PubMed abstract:  In the mammalian eye, the ON-centre and OFF-centre retinal ganglion cells form two major pathways projecting to central visual structures from the retina. These two pathways originate at the bipolar cell level: one class of bipolar cells becomes hyperpolarized in response to light, as do all photoreceptor cells, and the other class becomes depolarized on exposure to light, thereby inverting the receptor signal. It has recently become possible to examine the functional role of the ON-pathway in vision by selectively blocking it at the bipolar cell level using the glutamate neurotransmitter analogue 2-amino-4-phosphonobutyrate (APB)1. APB application to monkey, cat and rabbit retinas abolishes ON responses in retinal ganglion cells, the lateral geniculate nucleus and the visual cortex but has no effect on the centre-surround antagonism of OFF cells or the orientation and direction selectivities in the cortex2-5. These and related findings6-11 suggest that the ON and OFF pathways remain largely separate through the lateral geniculate nucleus and that in the cortex, contrary to some hypotheses, they are not directly involved in mechanisms giving rise to orientation and direction selectivities. We have examined the roles of the ON and OFF channels in vision in rhesus monkeys trained to do visual detection and discrimination tasks. We report here that the ON channel is reversibly blocked by injection of APB into the vitreous. Detection of light increment but not of light decrement is severely impaired, and there is a pronounced loss in contrast sensitivity. The perception of shape, colour, flicker, movement and stereo images is only mildly impaired, but longer times are required for their discrimination. Our results suggest that two reasons that the mammalian visual system has both ON and OFF channels is to yield equal sensitivity and rapid information transfer for both incremental and decremental light stimuli and to facilitate high contrast sensitivity.

Research Reports:

Adelson, E. H. "Perceptual Organization and the Judgment of Brightness." Science 262 (1993): 2042-2044.

PubMed abstract:  The perceived brightness of a gray patch depends on the surrounding context. For example, a medium-gray patch appears darker when placed on a bright background and brighter when placed on a dark background. Models to explain these effects are usually based on simple low-level mechanisms. A new set of brightness illusions cannot be explained by such models. In these illusions, the brightness percept is strongly influenced by the perceptual organization of the stimuli. Simple modifications of the stimuli that should have little effect on low-level mechanisms greatly alter the strength of the illusion. These effects may be ascribed to more complex mechanisms occurring later in the visual system.

Rossi, A. F., C. D. Rittenhouse, and M. A. Paradiso. "The Representation of Brightness in Primary Visual Cortex." Science 273 (1996): 1104-7.

PubMed abstract:  Although neurons in primary visual cortex are sensitive to the spatial distribution and intensity of light, their responses have not been thought to correlate with the perception of brightness. Indeed, primary visual cortex is often described as an initial processing stage that sends information to higher cortical areas where perception of brightness, color, and form occurs. However, a significant percentage of neurons in primary visual cortex were shown to respond in a manner correlated with perceived brightness, rather than responding strictly to the light level in the receptive fields of the cells. This finding suggests that even at the first stage of visual cortical processing, spatial integration of information yields perceptual qualities that are only indirectly related to the pattern of illumination of the retina.

Assigned Readings:

Livingstone, M., and D. H. Hubel. "Segregation of Form, Color, Movement and Depth: Anatomy, Physiology and Perception." Science 240 (1988): 740-749.

PubMed abstract:  Anatomical and physiological observations in monkeys indicate that the primate visual system consists of several separate and independent subdivisions that analyze different aspects of the same retinal image: cells in cortical visual areas 1 and 2 and higher visual areas are segregated into three interdigitating subdivisions that differ in their selectivity for color, stereopsis, movement, and orientation. The pathways selective for form and color seem to be derived mainly from the parvocellular geniculate subdivisions, the depth- and movement-selective components from the magnocellular. At lower levels, in the retina and in the geniculate, cells in these two subdivisions differ in their color selectivity, contrast sensitivity, temporal properties, and spatial resolution. These major differences in the properties of cells at lower levels in each of the subdivisions led to the prediction that different visual functions, such as color, depth, movement, and form perception, should exhibit corresponding differences. Human perceptual experiments are remarkably consistent with these predictions. Moreover, perceptual experiments can be designed to ask which subdivisions of the system are responsible for particular visual abilities, such as figure/ground discrimination or perception of depth from perspective or relative movement--functions that might be difficult to deduce from single-cell response properties.

Schiller, P. H., N. K. Logothetis, and E. R. Charles. "The Role of the Color-opponent and Broad-band Channels in Vision." Visual Neuroscience 5 (1990): 321-346.

PubMed abstract:  The functions of the primate color-opponent and broad-band channels were assessed by examining the visual capacities of rhesus monkeys following selective lesions of parvocellular and magnocellular lateral geniculate nucleus, which respectively relay these two channels to the cortex. Parvocellular lesions impaired color vision, high spatial-frequency form vision, and fine stereopsis. Magnocellular lesions impaired high temporal-frequency flicker and motion perception but produced no deficits in stereopsis. Low spatial-frequency form vision, stereopsis, and brightness perception were unaffected by either lesion. Much as the rods and cones of the retina can be thought of as extending the range of vision in the intensity domain, we propose that the color-opponent channel extends visual capacities in the wavelength and spatial-frequency domains whereas the broad-band channel extends them in the temporal domain

Schiller, P. H., and N. K. Logothetis. "The Color-opponent and Broad-band Channels of the Primate." Trends in Neurosciences 13 (1990): 392-398.

Research Reports:

Maunsell, J. H. R, T. A. Nealy, and D. D. DePriest. "Magnocellular and Parovcellular Contributions to Responses in the Middle Temporal Area (MT) of the Macaque Monkey." J. Neurosci. 10 (1990): 3323-3334.

PubMed abstract:  Many lines of evidence suggest that the visual signals relayed through the magnocellular and parvocellular subdivisions of the primate dorsal LGN remain largely segregated through several levels of cortical processing. It has been suggested that this segregation persists through to the highest stages of the visual cortex, and that the pronounced differences between the neuronal response properties in the parietal cortex and inferotemporal cortex may be attributed to differential contributions from magnocellular and parvocellular signals. We have examined this hypothesis directly by recording the responses of cortical neurons while selectively blocking responses in the magnocellular or parvocellular layers of the LGN. Responses were recorded from single units or multiunit clusters in the middle temporal visual area (MT), which is part of the pathway leading to parietal cortex and thought to receive primarily magnocellular inputs. Responses in the MT were consistently reduced when the magnocellular subdivision of the LGN was inactivated. The reduction was almost always pronounced and often complete. In contrast, parvocellular block rarely produced striking changes in MT responses and typically had very little effect. Nevertheless, unequivocal parvocellular contributions could be demonstrated for a minority of MT responses. At a few MT sites, responses were recorded while magnocellular and parvocellular blocks were made simultaneously. Responses were essentially eliminated for all these paired blocks. These results provide direct evidence for segregation of magnocellular and parvocellular contributions in the extrastriate visual cortex and support the suggestion that these signals remain largely segregated through the highest levels of cortical processing.

Ferrera, V. P., T. A. Nealy, and J. H. R. Maunsell. "Mixed Parvocellular and Magnocellular Geniculate Signals in Visual Area V4." Nature 358 (1992): 756-758.

PubMed abstract:  Visual information from the retina is transmitted to the cerebral cortex by way of the lateral geniculate nucleus (LGN) in the thalamus. In primates, most of the retinal ganglion cells that project to the LGN belong to one of two classes, P and M, whose axons terminate in the parvocellular or magnocellular subdivisions of the LGN. These cell classes give rise to two channels that have been distinguished anatomically, physiologically and behaviourally. The visual cortex also can be subdivided into two pathways, one specialized for motion processing and the other for colour and form information. Several lines of indirect evidence have suggested a close correspondence between the subcortical and cortical pathways, such that the M channel provides input to the motion pathway and the P channel drives the colour/form pathway. This hypothesis was tested directly by selectively inactivating either the magnocellular or parvocellular subdivision of the LGN and recording the effects on visual responses in the cortex. We have previously reported that, in accordance with the hypothesis, responses in the motion pathway in the cortex depend primarily on magnocellular LGN. We now report that in the colour/form pathway, visual responses depend on both P and M input. These results argue against a simple correspondence between the subcortical and cortical pathways.

Assigned Readings:

Derrington, A. M., J. Krauskopf, and P. Lennie. "Chromatic Mechanisms in Lateral Geniculate Nucleus of Macaque." J. Physiol. 357 (1984): 241-265.

PubMed abstract:  This paper introduces a new technique for the analysis of the chromatic properties of neurones, and applies it to cells in the lateral geniculate nucleus (l.g.n.) of macaque. The method exploits the fact that for any cell that combines linearly the signals from cones there is a restricted set of lights to which it is equally sensitive, and whose members can be exchanged for one another without evoking a response. Stimuli are represented in a three-dimensional space defined by an axis along which only luminance varies, without change in chromaticity, a 'constant B' axis along which chromaticity varies without changing the excitation of blue-sensitive (B) cones, a 'constant R & G' axis along which chromaticity varies without change in the excitation of red-sensitive (R) or green-sensitive (G) cones. The orthogonal axes intersect at a white point. The isoluminant plane defined by the intersection of the 'constant B' and 'constant R & G' axes contains lights that vary only in chromaticity. In polar coordinates the constant B axis is assigned the azimuth 0-180 deg, and the constant R & G axis the azimuth 90-270 deg. Luminance is expressed as elevation above or below the isoluminant plane (-90 to +90 deg). For any cell that combines cone signals linearly, there is one plane in this space, passing through the white point, that contains all lights that can be exchanged silently. The position of this 'null plane' provides the 'signature' of the cell, and is specified by its azimuth (the direction in which it intersects the isoluminant plane of the stimulus space) and its elevation (its angle of inclination to the isoluminant plane). A colour television receiver was used to produce sinusoidal gratings whose chromaticity and luminance could be modulated along any vector passing through the white point in the space described. The spatial and temporal frequencies of modulation could be varied over a large range. When stimulated by patterns of low spatial and low temporal frequency, two groups of cells in the parvocellular laminae of the l.g.n. were distinguished by the locations of their null planes. The null planes of the larger group were narrowly distributed about an azimuth of 92.6 deg and more broadly about an elevation of 51.5 deg, which suggests that they receive opposed, but not equally balanced, inputs from only R and G cones. These we call R-G cells.

Dacey, D. M. "Parallel Pathways for Spectral Coding in Primate Retina." Annu. Rev. Neurosci. 23 (2000): 743-775.

PubMed abstract:  The primate retina is an exciting focus in neuroscience, where recent data from molecular genetics, adaptive optics, anatomy, and physiology, together with measures of human visual performance, are converging to provide new insights into the retinal origins of color vision. Trichromatic color vision begins when the image is sampled by short- (S), middle- (M) and long- (L) wavelength-sensitive cone photoreceptors. Diverse retinal cell types combine the cone signals to create separate luminance, red-green, and blue-yellow pathways. Each pathway is associated with distinctive retinal architectures. Thus a blue-yellow pathway originates in a bistratified ganglion cell type and associated interneurons that combine excitation from S cones and inhibition from L and M cones. By contrast, a red-green pathway, in which signals from L and M cones are opposed, is associated with the specialized anatomy of the primate fovea, in which the "midget" ganglion cells receive dominant excitatory input from a single L or M cone.

Schiller, P. H. "The Effects of V4 and Middle Temporal (MT) Area Lesions on Visual Performance in the Rhesus Monkey." Visual Neuroscience 10 (1993): 717-746.
(Read the following section: pp. 733-4, "Perception at Isoluminance" (Figs 19 and 20)).

PubMed abstract:  The effects of V4, MT, and combined V4 + MT lesions were assessed on a broad range of visual capacities that included measures of contrast sensitivity, wavelength and brightness discrimination, form vision, pattern vision, motion and flicker perception, stereopsis, and the selection of stimuli that were less prominent than those with which they appeared in stimulus arrays. The major deficit observed was a loss in the ability, after V4 lesions, to select such less prominent stimuli; this was the case irrespective of the manner in which the stimulus arrays were made visible, using either luminance, chrominance, motion, or stereoscopic depth as surface media. In addition, V4 lesions yielded mild deficits in color, brightness, and form vision whereas MT lesions yielded mild to moderate deficits in motion and flicker perception. Both lesions produced mild deficits in contrast sensitivity, shape-from-motion perception, and yielded increased reaction times on many of the tasks. The impairment resulting from combined V4 and MT lesions was not greater than the sum of the deficits of either lesion. None of the lesions produced significant deficits in stereopsis. The findings suggest that (1) area V4 is part of a neural system that is involved in extracting stimuli from the visual scene that elicit less neural activity early in the visual system than do other stimuli with which they appear and (2) several other extrastriate regions and more than just two major cortical processing streams contribute to the processing of basic visual functions in the extrastriate cortex.

Recommended Readings:

Kaiser, P. H., and R. M. Boynton. "The Encoding of Color." Chap. 7 in Human Color Vision. Optical Society of America, 1996.

Sekuler, R., and R. Blake. "Color Perception." Chap. 6 in Perception. McGraw-Hill, 1994.

Schiller, P. H. "Area V4 of the Primate Visual Cortex." Current Directions in Psychological Science 3 (1994): 89-92.

Schiller, P. H., N. K. Logothetis, and E. R. Charles. "Parallel Pathways in the Visual System: Their Role in Perception at Isoluminance." J. Neuropsychologia 29 (1991): 433-441.

PubMed abstract:  It has been proposed that the functions of the two major parallel channels of the primate visual system, the color-opponent and the broad-band, can be determined in psychophysical experiments by eliminating luminance but maintaining chrominance information (isoluminance), since under such conditions the broad-band channel is believed to be silenced. To test this proposition we examined the visual functions of monkeys after blocking either of these channels and we also assessed the responses of neurons to isoluminant stimuli in the lateral geniculate nucleus. We show that color, texture, stereopsis and pattern perception in the absence of the color-opponent channel, and flicker and motion perception in the absence of the broad-band channel are compromised. Yet isoluminance functions for stereopsis and texture in the absence of the broad-band channel and for motion in the absence of the color-opponent channel are indistinguishable from normal. Our recordings show that the neuronal responses of the broad-band cells for isoluminant exchange of red and green lights are reduced but not eliminated and that the color-opponent cells also become similarly less responsive under these conditions. We conclude that perceptual losses at isoluminance are not specific for either channel.

Research Reports:

Dacey, D. M., B. B. Lee, D. K. Stafford, J. Pokorny, and V. C. Smith. "Horizontal Cells of the Primate Retina: Cone Specificity without Spectral Opponency." Science 271 (1996): 656-9.

PubMed abstract:  The chromatic dimensions of human color vision have a neural basis in the retina. Ganglion cells, the output neurons of the retina, exhibit spectral opponency; they are excited by some wavelengths and inhibited by others. The hypothesis that the opponent circuitry emerges from selective connections between horizontal cell interneurons and cone photoreceptors sensitive to long, middle, and short wavelengths (L-, M-, and S-cones) was tested by physiologically and anatomically characterizing cone connections of horizontal cell mosaics in macaque monkeys. H1 horizontal cells received input only from L- and M-cones, whereas H2 horizontal cells received a strong input from S-cones and a weaker input from L- and M-cones. All cone inputs were the same sign, and both horizontal cell types lacked opponency. Despite cone type selectivity, the horizontal cell cannot be the locus of an opponent transformation in primates, including humans.

Chichilnisky, E. J., and D. A. Baylor. "Receptive-field Microstructure of Blue-yellow Ganglion Cells in Primate Retina." Nature Neuroscience 2 (1999): 889-893.

PubMed abstract:  We examined the functional microcircuitry of cone inputs to blue-ON/yellow-OFF (BY) ganglion cells in the macaque retina using multielectrode recording. BY cells were identified by their ON responses to blue light and OFF responses to red or green light. Cone-isolating stimulation indicated that ON responses originated in short (S) wavelength-sensitive cones, whereas OFF responses originated in both long (L) and middle (M) wavelength-sensitive cones. Stimulation with fine spatial patterns revealed locations of individual S cones in BY cell receptive fields. Neighboring BY cells received common but unequal inputs from one or more S cones. Inputs from individual S cones differed in strength, indicating different synaptic weights, and summed approximately linearly to control BY cell firing.

Dacey, D. M., B. B. Peterson, F. R. Robinson, and P. D. Gamlin. "Fireworks in the Primate Retina: In Vitro Photodynamics Reveals Diverse LGN-projecting Ganglion Cell Types." Neuron 37 (2003): 15-27.

PubMed abstract:  Diverse cell types and parallel pathways are characteristic of the vertebrate nervous system, yet it remains a challenge to define the basic components of most neural structures. We describe a process termed retrograde photodynamics that allowed us to rapidly make the link between morphology, physiology, and connectivity for ganglion cells in the macaque retina that project to the lateral geniculate nucleus (LGN). Rhodamine dextran injected into the LGN was transported retrogradely and sequestered within the cytoplasm of ganglion cell bodies. Exposure of the retina to light in vitro liberated the tracer and allowed it to diffuse throughout the dendrites, revealing the cell's complete morphology. Eight previously unknown LGN-projecting cell types were identified. Cells could also be targeted in vitro for intracellular recording and physiological analysis. The photodynamic process was also observed in pyramidal cells in a rat neocortical slice.

Assigned Readings:

Spillman, L., and J. S. Werner. Visual Perception. Academic Press, 1990, Chap. 5.

MacLeod, D. I. A., and M. Hayhoe. "Rod Origin of Prolonged After Images." Science 185 (1976): 1171-1172.

Kaiser, P. K., and R. M. Boynton. "Sensitivity Regulation." Chap. 6 in Human Color Vision. Optical Society of America, 1996.

Schiller, P. H., and R. P. Dolan. "Visual Aftereffects and the Consequences of Visual System Lesions on their Perception in the Rhesus Monkey." Vis. Neurosci. 11 (1994): 643-665.

PubMed abstract:  This study examined the consequences of visual system lesions on visual aftereffects produced by achromatic stimuli of various luminance contrasts and chromatic stimuli of various wavelength compositions. The effects of repeated exposure to such adapting stimuli were assessed using probes whose luminance contrast and wavelength composition were systematically varied using both detection and discrimination paradigms. Interocular tests revealed that both peripheral and central mechanisms contribute to the visual aftereffects produced by the adapting stimulus arrays used in this study. Contrary to the hypothesis according to which the midget system of the retina is the conveyor of visual afterimages, we found that blocking this system with lesions of parvocellular lateral geniculate nucleus, through which the midget cells make their way to the striate cortex in primates, did not eliminate the visual aftereffects. It appears therefore that the parasol system of the retina, which courses through the magnocellular layers of the lateral geniculate nucleus to cortex, can convey the necessary signals for the generation of visual aftereffects. Lesions of areas V4 and MT did not have significant effects on the visual aftereffects studied suggesting that the central factors that contribute to the visual aftereffects occur either already in area V1 or are conveyed to higher centers through regions other than areas V4 and MT.

Recommended Readings:

Hood, D. C. "Lower-level Visual Processing and Models of Light Adaptation." Ann Rev Psychol. 49 (1998): 503-35.

PubMed abstract:  Before there was a formal discipline of psychology, there were attempts to understand the relationship between visual perception and retinal physiology. Today, there is still uncertainty about the extent to which even very basic behavioral data (called here candidates for lower-level processing) can be predicted based upon retinal processing. Here, a general framework is proposed for developing models of lower-level processing. It is argued that our knowledge of ganglion cell function and retinal mechanisms has advanced to the point where a model of lower-level processing should include a testable model of ganglion cell function. This model of ganglion cell function, combined with minimal assumptions about the role of the visual cortex, forms a model of lower-level processing. Basic behavioral and physiological descriptions of light adaptation are reviewed, and recent attempts to model lower-level processing are discussed.

Research Reports:

Martin, P. R., B. B. Lee, A. J. R. White, S. G. Solomon, and L. Ruttiger. "Chromatic Sensitivity of Ganglon Cells in the Peripheral Primate Retina." Nature 410 (2001): 933-936.

PubMed abstract:  Visual abilities change over the visual field. For example, our ability to detect movement is better in peripheral vision than in foveal vision, but colour discrimination is markedly worse. The deterioration of colour vision has been attributed to reduced colour specificity in cells of the midget, parvocellular (PC) visual pathway in the peripheral retina. We have measured the colour specificity (red-green chromatic modulation sensitivity) of PC cells at eccentricities between 20 and 50 degrees in the macaque retina. Here we show that most peripheral PC cells have red-green modulation sensitivity close to that of foveal PC cells. This result is incompatible with the view that PC pathway cells in peripheral retina make indiscriminate connections ('random wiring') with retinal circuits devoted to different spectral types of cone photoreceptors. We show that selective cone connections can be maintained by dendritic field anisotropy, consistent with the morphology of PC cell dendritic fields in peripheral retina. Our results also imply that postretinal mechanisms contribute to the psychophysically demonstrated deterioration of colour discrimination in the peripheral visual field.

Xiao, Y., Y. Wang, and D. J. Felleman. "A Spatially Organized Representation of Colour in Macaque Cortical Area V2." Nature 421 (2003): 535-539.

PubMed abstract:  Neurons responding selectively to different colours have been found in various cortical areas in macaque monkeys; however, little is known about whether and how the representation of colour is spatially organized in any cortical area. Cortical area V2 contains modules that respond preferentially to chromatic modulation, which are located in thin cytochrome oxidase stripes. Here we show that within and beyond these modules, gratings of different colours produce activations that peak at different locations. Optical recording of intrinsic signals revealed that the peak regions of the responses to different colours were spatially organized in the same order as colour stimuli are arranged in the DIN (German standard colour chart) colour system. Nearby regions represented colours of a similar hue. We found that the set of colour-specific regions formed 0.07-0.32-mm-wide and approximately 1.3-mm long bands that varied in shape from linear to nearly circular. Our finding suggests that thin stripes in V2 contain functional maps where the colour of a stimulus is represented by the location of its response activation peak.

Webster, M. A., and J. D. Mollon. "Changes in Colour Appearance Following Post-receptoral Adaptation." Nature 349 (1991): 235-238.

PubMed abstract:  Current models of colour vision assume that colour is represented by activity in three independent post-receptoral channels: two encoding chromatic information and one encoding luminance. An important feature of these models is that variations in certain directions in colour space modulate the response of only one of the channels. We have tested whether such models can predict how colour appearance is altered by adaptation-induced changes in post-receptoral sensitivity. In contrast to the changes predicted by three independent channels, colour appearance is always distorted away from the direction in colour space to which the observer has adapted. This suggests that at the level at which the adaptation effects occur, there is no colour direction that invariably isolates only a single post-receptoral channel.

Arshavsky, V. Y. "Like Night and Day: Rods and Cones have Different Pigment Regeneration Pathways." Neuron 36 (2002): 1-4.

Sustained vision requires continuous regeneration of visual pigments in rod and cone photoreceptors by the 11-cis-retinal chromophore. In this issue of Neuron, Mata et al. report a novel enzymatic pathway uniquely designed to keep up with the high demand for cone pigment regeneration in bright light and to preclude rods from utilizing chromophore produced in daylight, when rods are not very useful for vision.

Recommended Readings for Background:

Schiller, P. H. "The Central Visual System." Vision Research 26. (Read section on the tectal system, pp.1372-1377.)

Assigned Readings:

Schiller, P. H. "The Neural Control of Visually Guided Eye Movements." In Cognitive Neuroscience of Attention. Edited by J. Richards. Erlbaum, 1998.

Research Reports:

Hikosaka, O., and R. H. Wurtz. "Modification of Saccadic Eye Movements by GABA-Related Substances. I. Effect of Muscimol and Bicuculine in Monkey Superior Colliculus." J. Neurophysiol. 53 (1985): 266-291.

PubMed abstract:  Our previous observations led to the hypothesis that cells in the substantia nigra pars reticulata (SNr) tonically inhibit saccade-related cells in the intermediate layers of the superior colliculus (SC). Before saccades to visual or remembered targets, cells in SNr briefly reduce that inhibition, allowing a burst of spikes of SC cells that, in turn, leads to the initiation of a saccadic eye movement. Since this inhibition is likely to be mediated by gamma-aminobutyric acid (GABA), we tested this hypothesis by injecting a GABA agonist (muscimol) or a GABA antagonist (bicuculline) into the superior colliculus and measured the effects on saccadic eye movements made to visual or remembered targets. An injection of muscimol selectively suppressed saccades to the movement field of the cells near the injection site. The affected area expanded over time, thus suggesting the diffusion of muscimol in the SC; the area never included the other hemifield, suggesting that the diffusion was limited to one SC. One of the monkeys became unable to make any saccades to the affected area. Saccades to visual targets following injection of muscimol had longer latency and slightly shorter amplitudes that were corrected by subsequent saccades. The most striking change was a decrease in the peak velocity of the saccade, frequently to less than half the preinjection value. Saccades to remembered targets following injection of muscimol also showed an increase in latency and decrease in velocity, but in addition, showed a striking decrease in the accuracy of the saccades. The trajectories of saccades became distorted as if they were deflected away from the affected area. After muscimol injection, the area over which spontaneous eye movements were made shifted toward the side ipsilateral to the injection. Saccades toward the contralateral side were less frequent and slower. In nystagmus, which developed later, the slow phase was toward the contralateral side. In contrast to muscimol, injection of bicuculline facilitated the initiation of saccades. Injection was followed almost immediately by stereotyped and apparently irrepressible saccades made toward the center of the movement field of the SC cells at the injection site. The monkeys became unable to fixate during the tasks; the fixation was interrupted by saccadic jerks made to the affected area of the visual field and then back to the fixation point.

Hikosaka, O., and R. H. Wurtz. "Modification of Saccadic Eye Movements by GABA-Related Substances. II. Effects of Muscimol in Monkey Substantia Nigra Pars Reticulata." J. Neurophysiol. 53 (1985): 292-308.

PubMed abstract:  The preceding study (21) showed that a gamma-aminobutyric acid (GABA) agonist or antagonist injected into the superior colliculus (SC) disrupted saccadic eye movements. The purpose of the present experiments was to determine whether this result was due to altering the inhibitory input to the SC from the substantia nigra pars reticulata (SNr). SNr cells are themselves inhibited by GABA. Injection of muscimol, a GABA agonist, into the SNr should increase the inhibition acting on SNr cells and should reduce the inhibition acting on the SC. If the effects of GABA inhibition in the SC results from terminals originating in the SNr, muscimol in the SNr should act like bicuculline in the SC. Muscimol in the SNr has the same general effect as bicuculline in the SC. The monkey made irrepressible saccades toward the contralateral visual field where cells in the SNr at the injection site had their visual or movement field. During visual fixation saccadic jerks occurred, interspersed with spontaneous saccades, instead of saccades to visual targets or to remembered targets. Saccades to remembered targets were more vulnerable to these saccadic intrusions than were saccades to visual targets. Since muscimol in the SNr acts like bicuculline in the SC, we conclude that a substantial fraction of GABA-mediated inhibitory inputs in the SC originates from the SNr. These experiments, in conjunction with previous experiments, show that the SNr exerts a tonic inhibition on saccade-related cells in SC and that this inhibition is mediated by GABA. The role of the SNr in initiation of saccades to remembered targets is particularly important since these saccades are more severely disrupted by muscimol in the SNr as well as in the SC. We suggest that both of these conclusions about eye movement might apply to skeletal movements as well. First, the basal ganglia contribute to the initiation of movement by a release of the target structure from tonic inhibition. Second, this mechanism is particularly critical of the movements based on stored or remembered signals that are not currently available as incoming sensory inputs.

Assigned Readings:

Schiller, P. H., and I. Chou. "The Effect of Frontal Eye Field and Dorsomedial Frontal Cortex Lesions on Visually Guided Eye Movements." Nature Neuroscience 1 (1998): 248-253.

PubMed abstract:  In the frontal lobe of primates, two areas play a role in visually guided eye movements: the frontal eye fields (FEF) and the medial eye fields (MEF) in dorsomedial frontal cortex. Previously, FEF lesions have revealed only mild deficits in saccadic eye movements that recovered rapidly. Deficits in eye movements after MEF ablation have not been shown. We report the effects of ablating these areas singly or in combination, using tests in which animals were trained to make saccadic eye movements to paired or multiple targets presented at various temporal asynchronies. FEF lesions produced large and long-lasting deficits on both tasks. Sequences of eye movements made to successively presented targets were also impaired. Much smaller deficits were observed after MEF lesions. Our findings indicate a major, long-lasting loss in temporal ordering and processing speed for visually guided saccadic eye movement generation after FEF lesions and a significant but smaller and shorter-lasting loss after MEF lesions.

Tehovnik, E. J., W. M. Slocum, and P. H. Schiller. "Differential Effects of Laminar Stimulation of V1 Cortex on Target Selection by Macaque Monkeys." European Journal of Neuroscience 16 (2002): 751-760.

Tehovnik, E. J., M. A. Sommer, I. Chou, W. M. Slocum, and P. H. Schiller. "Eye Fields in the Frontal Lobes of Primates." Brain Research Reviews 32 (2000): 413-448.

PubMed abstract:  Two eye fields have been identified in the frontal lobes of primates: one is situated dorsomedially within the frontal cortex and will be referred to as the eye field within the dorsomedial frontal cortex (DMFC); the other resides dorsolaterally within the frontal cortex and is commonly referred to as the frontal eye field (FEF). This review documents the similarities and differences between these eye fields. Although the DMFC and FEF are both active during the execution of saccadic and smooth pursuit eye movements, the FEF is more dedicated to these functions. Lesions of DMFC minimally affect the production of most types of saccadic eye movements and have no effect on the execution of smooth pursuit eye movements. In contrast, lesions of the FEF produce deficits in generating saccades to briefly presented targets, in the production of saccades to two or more sequentially presented targets, in the selection of simultaneously presented targets, and in the execution of smooth pursuit eye movements. For the most part, these deficits are prevalent in both monkeys and humans. Single-unit recording experiments have shown that the DMFC contains neurons that mediate both limb and eye movements, whereas the FEF seems to be involved in the execution of eye movements only. Imaging experiments conducted on humans have corroborated these findings. A feature that distinguishes the DMFC from the FEF is that the DMFC contains a somatotopic map with eyes represented rostrally and hindlimbs represented caudally; the FEF has no such topography. Furthermore, experiments have revealed that the DMFC tends to contain a craniotopic (i.e., head-centered) code for the execution of saccadic eye movements, whereas the FEF contains a retinotopic (i.e., eye-centered) code for the elicitation of saccades. Imaging and unit recording data suggest that the DMFC is more involved in the learning of new tasks than is the FEF. Also with continued training on behavioural tasks the responsivity of the DMFC tends to drop. Accordingly, the DMFC is more involved in learning operations whereas the FEF is more specialized for the execution of saccadic and smooth pursuit eye movements.

Schiller, P. H., and J. E. Tehovnik. "Look and See: How the Brain Moves Your Eyes About." Chap. 9 in Vision: from Neurons to Cognition. Edited by C. Casanova, and M. Ptito. Progress in Brain Research 134, Amsterdam, Elsevier.

PubMed abstract:  Two major cortical streams are involved in the generation of visually guided saccadic eye movements: the anterior and the posterior. The anterior stream from the frontal and medial eye fields has direct access to brainstem oculomotor centers. The posterior stream from the occipital cortices reaches brainstem oculomotor centers through the superior colliculus. The parietal cortex interconnects with both streams. Our findings suggest that the posterior stream plays an unique role in the execution of rapid, short-latency eye movements called 'express saccades'. Both the anterior and posterior streams play a role in the selection of targets to which saccades are to be generated, but do so in different ways. Areas V1, V2 and LIP contribute to decisions involved in where to look as well as where not to look. In addition, area LIP is involved in decisions about how long to maintain fixation prior to the execution of a saccade. Area V4 does not appear to be directly involved in eye-movement generation. In the anterior stream, the frontal eye fields, and to a lesser extent the medial eye fields, are involved in the correct execution of saccades subsequent to decisions made about where to look and where not to look.

Assigned Readings:

Background: Schiller, P. H. "The Central Visual System." Vision Research 26 (1986). (Read section on the accessory optic system, pp. 1377-1378.) 

Albright, T. D. "Form-cue Invariant Motion Processing in Primate Visual Cortex." Science 255 (1991): 1141-1143.

Duffy, C. J., and R. H. Wurtz. "Sensitivity of MST Neurons to Optic Flow Stimuli. I. A Continuum of Response Selectivity to Large-field Stimuli." J. Neurophysiol. 65 (1991): 1329-1345.

PubMed abstract:  Neurons in the dorsomedial region of the medial superior temporal area (MSTd) have large receptive fields that include the fovea, are directionally selective for moving visual stimuli, prefer the motion of large fields to small spots, and respond to rotating and expanding patterns of motion as well as frontal parallel planar motion. These characteristics suggested that these neurons might contribute to the analysis of the large-field optic flow stimulation generated as an observer moves through the visual environment. 2. We tested the response of MSTd neurons in two awake monkeys by systematically presenting a set of translational and rotational stimuli to each neuron. These 100 X 100 degrees stimuli were the motion components from which all optic flow fields are derived. 3. In 220 single neurons we found 23% that responded primarily to one component of motion (planar, circular, or radial), 34% that responded to two components (planocircular or planoradial, but never circuloradial), and 29% that responded to all three components. 4. The number of stimulus components to which a neuron responded was unrelated to the size or eccentricity of its receptive field. 5. Triple-, double-, and single-component neurons varied widely in the strength of their responses to the preferred components. Grouping these neurons together revealed that they did not form discrete classes but rather a continuum of response selectivity. 6. This continuum was apparent in other response characteristics. Direction selectivity was weakest in triple-component neurons, strongest in single-component neurons. Significant inhibitory responses were less frequent in triple-component neurons than in single-component neurons. 7. There was some indication that the neurons of similar component classes occupied adjacent regions within MSTd, but all combinations of component and direction selectivity were occasionally found in immediate juxtaposition. 8. Experiments on a subset of neurons showed that the speed of motion, the dot density, and the number of different speed planes in the display had little influence on these responses. 9. We conclude that the selective responses of many MSTd neurons to the rotational and translational components of optic flow make these neurons reasonable candidates for contributing to the analysis of optic flow fields.

Duffy, C. J., and R. H. Wurtz. "Response of Monkey MST Neurons to Optic Flow Stimuli with Shifted Centers of Motion." J. Neurosci. 15 (1995): 5192-5208.

PubMed abstract:  Neurons in the dorsal region of the medial superior temporal area (MSTd) have previously been shown to respond to the expanding radial motion that occurs as an observer moves through the environment. In previous experiments, MSTd neurons were tested with radial and circular motion centered in the visual field. However, different directions of observer motion, relative to the direction of gaze, are accompanied by visual motion centered at different locations in the visual field. The present experiments investigated whether neurons that respond to radial and circular motion might respond differently when the center of motion was shifted to different regions of the visual field. About 90% of the 245 neurons studied responded differently when the center of motion was shifted away from the center of the field. The centers of motion preferred by each neuron were limited to one area of the visual field. All parts of the visual field were represented in the sample, with greater numbers of neurons preferring centers of motion closer to the center of the field. We hypothesize that each of the MSTd neurons has a center of motion field with a gradient of preferred centers of motion, and that there is an orderly arrangement of MSTd neurons with each region of the visual field being represented by a set of neurons. This arrangement creates the potential for graded responses from individual neurons for different directions of heading as an observer moves through the environment.

Recommended Readings:

Salzman, C. D., and W. T. Newsome. "Neural Mechanisms for Forming a Perceptual Decision." Science 264 (1994): 231-237.

PubMed abstract:  Cognitive and behavioral responses to environmental stimuli depend on an evaluation of sensory signals within the cerebral cortex. The mechanism by which this occurs in a specific visual task was investigated with a combination of physiological and psychophysical techniques. Rhesus monkeys discriminated among eight possible directions of motion while directional signals were manipulated in visual area MT. One directional signal was generated by a visual stimulus and a second signal was introduced by electrically stimulating neurons that encoded a specific direction of motion. The decisions made by the monkeys in response to the two signals allowed a distinction to be made between two possible mechanisms for interpreting directional signals in MT. The monkeys tended to cast decisions in favor of one or the other signal, indicating that the signals exerted independent effects on performance and that an interactive mechanism such as vector averaging of the two signals was not operative. Thus, the data suggest a mechanism in which monkeys chose the direction encoded by the largest signal in the representation of motion direction, a "winner-take-all" decision process.

Nakayama, K. "Biological Image Motion Processing: A Review." Vis. Res. 25 (1985): 625-660.

Research Reports:

Stoner, G. R., T. D. Albright, and V. S. Ramachandran. "Transparency and Coherence in Human Motion Perception." Nature 344 (1990): 153-155.

PubMed abstract:  When confronted with moving images, the visual system often must decide whether the motion signals arise from a single object or from multiple objects. A special case of this problem arises when two independently moving gratings are superimposed. The gratings tend to cohere and move unambiguously in a single direction (pattern motion) instead of moving independently (component motion). Here we report that the tendency to see pattern motion depends very strongly on the luminance of the intersections (that is, to regions where the gratings overlap) relative to that of the gratings in a way that closely parallels the physics of transparency. When the luminance of these regions is chosen appropriately, pattern motion is destroyed and replaced by the appearance of two transparent gratings moving independently. The observations imply that motion detecting mechanisms in the visual system must have access to tacit 'knowledge' of the physics of transparency and that this knowledge can be used to segment the scene into different objects. The same knowledge could, in principle, be used to avoid confusing shadows with real object boundaries.

Fukushima, K., T. Yamanobe, Y. Shinmei, J. Fukushima, S. Kurkin, and B. W. Peterson. "Coding of Smooth Eye Movements in Three-dimensional Space by Frontal Cortex." Nature 419 (2002): 157-162.

PubMed abstract:  Through the development of a high-acuity fovea, primates with frontal eyes have acquired the ability to use binocular eye movements to track small objects moving in space. The smooth-pursuit system moves both eyes in the same direction to track movement in the frontal plane (frontal pursuit), whereas the vergence system moves left and right eyes in opposite directions to track targets moving towards or away from the observer (vergence tracking). In the cerebral cortex and brainstem, signals related to vergence eye movements--and the retinal disparity and blur signals that elicit them--are coded independently of signals related to frontal pursuit. Here we show that these types of signal are represented in a completely different way in the smooth-pursuit region of the frontal eye fields. Neurons of the frontal eye field modulate strongly during both frontal pursuit and vergence tracking, which results in three-dimensional cartesian representations of eye movements. We propose that the brain creates this distinctly different intermediate representation to allow these neurons to function as part of a system that enables primates to track and manipulate objects moving in three-dimensional space.

Gamlin, P. D., and K. Yoon. "An Area for Vergence Eye Movement in Primate Frontal Cortex." Nature 407 (2000): 1003-1007.

PubMed abstract:  To view objects at different distances, humans rely on vergence eye movements to appropriately converge or diverge the eyes and on ocular accommodation to focus the object. Despite the importance of these coordinated eye movements (the 'near response') very little is known about the role of the cerebral cortex in their control. As near-response neurons exist within the nucleus reticularis tegmenti pontis, which receives input from the frontal eye field region of frontal cortex, and this cortical region is known to be involved in saccadic and smooth-pursuit eye movements, we propose that a nearby region might play a role in vergence and ocular accommodation. Here we provide evidence from rhesus monkeys that a region of frontal cortex located immediately anterior to the saccade-related frontal eye field region is involved in vergence and ocular accommodation, and in the sensorimotor transformations required for these eye movements. We conclude that the macaque frontal cortex is involved in the control of all voluntary eye movements, and suggest that the definition of the frontal eye fields should be expanded to include this region.

Assigned Readings:

Howard, I. P., and B. J. Rogers. "Tests of Stereopsis" (pp. 149-155), "Motion Parallax" (pp. 571-584), and "Stereo in Animals" (chap. 16, pp. 645-657). In Binocular Vision and Stereopsis. Oxford University Press, 1995.

Parker, A. J., and B. G. Cumming. "Cortical Mechanisms of Binocular Stereoscopic Vision." Chap. 14 in Vision: from Neurons to Cognition. Edited by C. Casanova, and M. Ptito. Progress in Brain Research 134, Amsterdam, Elsevier, 2001.

PubMed abstract:  The early neurophysiology of binocular vision is largely dominated by measurements of disparity selectivity in cortical neurons in various visual areas. Incisive progress has been made by the intensive study of the mechanism of disparity selectivity of V1 in cortical neurons and the development of a number of tests for the involvement of single neurons in the perception of stereoscopic depth. The picture that now emerges is that cortical area V1 must be a preliminary processing stage for the analysis of stereoscopic depth, whereas some of the extrastriate areas may actually be responsible for the generation of neuronal signals that underlie the perception of binocular depth.

Poggio, G. F., F. Gonzalez, and F. Krause. "Stereoscopic Mechanisms in Monkey Visual Cortex: Binocular Correlation and Disparity Selectivity." J. Neurosci. 8 (1989): 4531-4551.

Schiller, P. H., N. K. Logothetis, and E. R. Charles. "The Role of the Color-opponent and Broad-band Channels in Vision." Visual Neuroscience 5 (1990): 321-346. (Read material pertaining to Figs. 22, 23 and 24.)

PubMed abstract:  The functions of the primate color-opponent and broad-band channels were assessed by examining the visual capacities of rhesus monkeys following selective lesions of parvocellular and magnocellular lateral geniculate nucleus, which respectively relay these two channels to the cortex. Parvocellular lesions impaired color vision, high spatial-frequency form vision, and fine stereopsis. Magnocellular lesions impaired high temporal-frequency flicker and motion perception but produced no deficits in stereopsis. Low spatial-frequency form vision, stereopsis, and brightness perception were unaffected by either lesion. Much as the rods and cones of the retina can be thought of as extending the range of vision in the intensity domain, we propose that the color-opponent channel extends visual capacities in the wavelength and spatial-frequency domains whereas the broad-band channel extends them in the temporal domain

Schiller, P.H. "The Effects of V4 and Middle Temporal (MT) Area Lesions on Visual Performance in the Rhesus Monkey." Visual Neuroscience 10 (1993): 717-746. (Read material pertaining to Figs. 18, 20, 25 and 28.)

PubMed abstract:  The effects of V4, MT, and combined V4 + MT lesions were assessed on a broad range of visual capacities that included measures of contrast sensitivity, wavelength and brightness discrimination, form vision, pattern vision, motion and flicker perception, stereopsis, and the selection of stimuli that were less prominent than those with which they appeared in stimulus arrays. The major deficit observed was a loss in the ability, after V4 lesions, to select such less prominent stimuli; this was the case irrespective of the manner in which the stimulus arrays were made visible, using either luminance, chrominance, motion, or stereoscopic depth as surface media. In addition, V4 lesions yielded mild deficits in color, brightness, and form vision whereas MT lesions yielded mild to moderate deficits in motion and flicker perception. Both lesions produced mild deficits in contrast sensitivity, shape-from-motion perception, and yielded increased reaction times on many of the tasks. The impairment resulting from combined V4 and MT lesions was not greater than the sum of the deficits of either lesion. None of the lesions produced significant deficits in stereopsis. The findings suggest that (1) area V4 is part of a neural system that is involved in extracting stimuli from the visual scene that elicit less neural activity early in the visual system than do other stimuli with which they appear and (2) several other extrastriate regions and more than just two major cortical processing streams contribute to the processing of basic visual functions in the extrastriate cortex.

Recommended Readings:

Sekuler, R., and R. Blake, eds. Perception. McGraw-Hill, chap. 7.

Spillman, L., and J. S. Werner, eds. Visual Perception. Academic Press, 1990, chap. 12.

Research Reports:

DeAngelis, G. C., B. G. Cumming, and W. T. Newsome. "Cortical Area MT and the Perception of Stereoscopic Depth." Nature 394 (1998): 677-680.

PubMed abstract:  Stereopsis is the perception of depth based on small positional differences between images formed on the two retinae (known as binocular disparity). Neurons that respond selectively to binocular disparity were first described three decades ago, and have since been observed in many visual areas of the primate brain, including V1, V2, V3, MT and MST. Although disparity-selective neurons are thought to form the neural substrate for stereopsis, the mere existence of disparity-selective neurons does not guarantee that they contribute to stereoscopic depth perception. Some disparity-selective neurons may play other roles, such as guiding vergence eye movements. Thus, the roles of different visual areas in stereopsis remain poorly defined. Here we show that visual area MT is important in stereoscopic vision: electrical stimulation of clusters of disparity-selective MT neurons can bias perceptual judgements of depth, and the bias is predictable from the disparity preference of neurons at the stimulation site. These results show that behaviourally relevant signals concerning stereoscopic depth are present in MT

Thomas, O. W., B. G. Cumming, and A. J. Parker. "A Specialization for Relative Disparity in V2." Nature Neuroscience 5 (2002): 472-478.

PubMed abstract:  Stereoscopic depth perception relies on binocular disparities, or small geometric differences between the retinal images of each eye. The most reliable binocular depth judgments are those that are based on relative disparities between two simultaneously visible features in a scene. Many cortical areas contain neurons that are sensitive to disparity, but it is unclear whether any areas show a specific sensitivity to relative disparity. We recorded from neurons in the early cortical visual area V2 of the awake macaque during presentation of random-dot patterns. The depth of a central region ('center'), and that of an annular surrounding region ('surround'), were manipulated independently in these stimuli. Some cells were fully selective for the resulting relative disparities. Most showed partial selectivity, which nonetheless indicated a sensitivity for the depth relationship between center and surround. Both types of neural response could support psychophysical judgments of relative depth.

Assigned Readings:

Schiller, P. H. "The Effects of V4 and Middle Temporal (MT) Area Lesions on Visual Performance in the Rhesus Monkey." Visual Neuroscience 10 (1993): 717-746. (Read material pertaining to Figs. 12, 13, 14, 21, 22, 23, 24, 25, 27 and 29.)

PubMed abstract:  The effects of V4, MT, and combined V4 + MT lesions were assessed on a broad range of visual capacities that included measures of contrast sensitivity, wavelength and brightness discrimination, form vision, pattern vision, motion and flicker perception, stereopsis, and the selection of stimuli that were less prominent than those with which they appeared in stimulus arrays. The major deficit observed was a loss in the ability, after V4 lesions, to select such less prominent stimuli; this was the case irrespective of the manner in which the stimulus arrays were made visible, using either luminance, chrominance, motion, or stereoscopic depth as surface media. In addition, V4 lesions yielded mild deficits in color, brightness, and form vision whereas MT lesions yielded mild to moderate deficits in motion and flicker perception. Both lesions produced mild deficits in contrast sensitivity, shape-from-motion perception, and yielded increased reaction times on many of the tasks. The impairment resulting from combined V4 and MT lesions was not greater than the sum of the deficits of either lesion. None of the lesions produced significant deficits in stereopsis. The findings suggest that (1) area V4 is part of a neural system that is involved in extracting stimuli from the visual scene that elicit less neural activity early in the visual system than do other stimuli with which they appear and (2) several other extrastriate regions and more than just two major cortical processing streams contribute to the processing of basic visual functions in the extrastriate cortex.

Schiller, P. H. "Past and Present Ideas About How the Visual Scene is Analyzed by the Brain." In Cerebral Cortex. Edited by Rockland, Kaas, and Peters. Plenum Press, 1997.

Von der Heydt, R., and E. Peterhans. "Mechanisms of Contour Perception in Monkey Visual Cortex: 1. Lines of Pattern Discontinuity." J. Neurosci. 9 (1989): 1731-1748.

PubMed abstract:  We have studied the mechanism of contour perception by recording from neurons in the visual cortex of alert rhesus monkeys. In order to assess the relationship between neural signals and perception, we compared the responses to edges and lines with the responses to patterns in which human observers perceive a contour where no line or edge is given (anomalous contour), such as the border between gratings of thin lines offset by half a cycle. With only one exception out of 60, orientation-selective neurons in area V1 did not signal the anomalous contour. Many neurons failed to respond to this stimulus at all, others responded according to the orientation of the grating lines. In area V2, 45 of 103 neurons (44%) signaled the orientation of the anomalous contour. Sixteen did so without signaling the orientation of the inducing lines. Some responded better to anomalous contours than to the optimum bars or edges. Preferred orientations and widths of tuning for anomalous contour and bar or edge were found to be highly correlated, but not identical, in each neuron. Similar to perception, the neuronal responses depended on a minimum number of lines inducing the contour, but not so much on line spacing, and tended to be weaker when the lines were oblique rather than orthogonal to the border. With oblique lines, the orientations signaled were biased towards the orientation orthogonal to the lines, as in the Zollner illusion. We conclude that contours may be defined first at the level of V2. While the unresponsiveness of neurons in V1 to this type of anomalous contour is in agreement with linear filter predictions, the responses of V2 neurons need to be explained. We assume that they sum the signals of 2 parallel paths, one that defines edges and lines and another that defines anomalous contours by pooling signals from end-stopped receptive fields oriented mainly orthogonal to the contour.

Schwartz, E. L. "Computational Studies of the Spatial Architecture of Primate Visual Cortex: Columns, Maps, and Protomaps." In Cerebral Cortex. Vol. 10. Edited by A. Peters, and K. S. Rockland. Plenum Press, New York, 1994.

Recommended Readings:

Sekuler, R., and R. Blake, eds. Perception. McGraw-Hill, chap. 5.