The ability to extract form information from a visual scene, for object recognition or figure–ground segregation, is a fundamental visual system function. Many studies of nonhuman primates have addressed the neural mechanisms involved in global form processing, but few have sought to demonstrate this ability behaviorally. In this study, we probed global visual processing in macaque monkeys (Macaca nemestrina) using classical Kanizsa illusory shapes as an assay of global form perception. We trained three monkeys on a “similarity match-to-sample” form discrimination task, first with complete forms embedded in fields of noncontour-inducing “pacman” elements. We then tested them with classic Kanizsa illusory shapes embedded in fields of randomly oriented elements. Two of the three subjects reached our criterion performance level of 80% correct or better on four of five illusory test conditions, demonstrating clear evidence of Kanizsa illusory form perception; the third subject mastered three of five conditions. Performance limits for illusory form discrimination were obtained by manipulating support ratio and by measuring threshold for discriminating “fat” and “thin” illusory squares. Our results indicate that macaque monkeys are capable of global form processing similarly to humans and that the perceptual mechanisms for “filling-in” contour gaps exist in macaques as they do in humans.

White noise stimuli were used to estimate second-order kernels for complex cells in cortical area VI of the macaque monkey, and drifting grating stimuli were presented to the same sample of neurons to obtain orientation and spatial-frequency tuning curves. Using these data, we quantified how well second-order kernels predict the normalized tuning of the average response of complex cells to drifting gratings.

The estimated second-order kernel of each complex cell was transformed into an interaction function defined over all spatial and temporal lags without regard to absolute position or delay. The Fourier transform of each interaction function was then computed to obtain an interaction spectrum. For a cell that is well modeled by a second-order system, the cell’s interaction spectrum is proportional to the tuning of its average spike rate to drifting gratings. This result was used to obtain spatial-frequency and orientation tuning predictions for each cell based on its second-order kernel. From the spatial-frequency and orientation tuning curves, we computed peaks and bandwidths, and an index for directional selectivity.

We found that the predictions derived from second-order kernels provide an accurate description of the change in the average spike rate of complex cells to single drifting sine–wave gratings. These findings are consistent with a model for complex cells that has a quadratic spectral energy operator at its core but are inconsistent with a spectral amplitude model.

Human, macaque monkey, and rat retinas were immunostained with a polyclonal antibody preparation against purified recoverin, a 23-kD calcium-binding protein isolated from bovine retina that localizes to rods and cones (Dizhoor et al., 1991). In addition to immunoreactive photoreceptors, we have identified subpopulations of recoverin-positive bipolar cells in all three species. Results from immunostaining with progressive dilutions of anti-recoverin and preadsorption of the antibody with a dilution series of purified recoverin showed that photoreceptors and bipolar cells had similar affinities for the antibody and suggested that the molecule recognized by the antibody in both cell types is recoverin. Immunoreactivity for recoverin and protein kinase C, a selective marker for all rod bipolar cells, was found in separate bipolar cell populations. Recoverin immunoreactivity is therefore a characteristic of certain cone bipolar cell types.

In rat retina, anti-recoverin labeled two morphologically distinct subpopulations of cone bipolar cells whose axonal arbors stratified at different depths in the inner plexiform layer (IPL). The bipolar cells labeled with anti-recoverin did not correspond to those that were reactive for calbindin, another cone bipolar cell marker.

Human and monkey retinas also had two populations of cone bipolar cells that were recoverin-positive. One population showed a distinct pattern of narrow bistratification at the outer border of the IPL and a regular mosaic arrangement of its axonal arbors, suggesting that the entire population of a single cone bipolar type was labeled. Cell density, dendritic morphology, and axonal-field size and stratification indicate that anti-recoverin selectively stains the flat midget (presumed OFF-center) cone bipolar cell type observed previously in Golgi preparations. By contrast the second bipolar cell population had axonal stratification in the inner half of the IPL and showed an unusual but consistent morphology and spatial distribution. Individual cells were intensely stained but were present at an extremely low density (~2−5 cells/mm2). These cells had multibranched dendritic trees characteristic of the diffuse bipolar cell class, but very small axonal fields in the size range of the midget bipolar class. Neither of the two recoverin-positive bipolar cell types in monkey was labeled with anti-calbindin or anti-cholecystokinin. An antibody preparation against bovine pineal hydroxyindole-O-methyltransferase (HIOMT) labeled photoreceptors and bipolar cells that closely resembled the recoverin-positive bipolar cells in human and rat retinas. Preadsorption of this antibody preparation with purified recoverin abolished immunostaining of the bipolar cells, suggesting that the anti-HIOMT preparation contains antibodies against recoverin, which is known to be present in the bovine pineal gland.

The activity of parietal cortex neurones primarily related to eye position (EP neurones) was studied in macaque monkeys with the aim of precisely defining the neurones' gaze fields (GF) and comparing them in two functionally different areas, MSTd and 7a. Discharge rates of single neurones in the inferior parietal lobule and in the underlying cortex of the superior temporal sulcus were recorded in two Java monkeys while the animals fixated a steady visual target positioned at several different points on a video screen. The GFs were then drawn as a regression surface fitting the mean discharge rates. Cells tonically influenced by the angle of gaze were found in both areas. The GFs most often took the form of a nearly planar surface best characterized as a ramp tilted towards a hemifield or quadrant of the visual field, shifted eccentrically with respect to the straight ahead (primary position), and with a midpoint centred between 0 deg and 20 deg of gaze eccentricity and saturation between 10 deg and 35 deg. In a minority of cases, the discharge rate was nearly maximal at the primary position and decreased to a minimum within 35 deg of eccentricity. In other instances, the GFs were peaked surfaces, limited to a restricted part of visual space. EP neurones, while showing similar gaze fields in areas MST and 7a, were found intermingled with functionally different types of cells. The results suggest that EP neurones similar to those already described in several areas of the monkey parietal cortex are present also in area MST. These cells, by signalling the degree of gaze eccentricity from the primary position, encode gaze position in an orbito-centered frame extending up to 30–35 deg from the straight-ahead. The role of EP neurones might be to supply contiguous elements with a gaze eccentricity signal required for visuo-motor processes such as the control of tracking movements.

Layers II/III of the primary visual cortex contain a regular pattern of histochemically detectable cytochrome oxidase (CO)-rich “puffs,” which differ from the interpuff regions in their thalamo-cortical and cortico-cortical connectivity, receptive-field properties, and the density of inhibitory GABA-containing synaptic terminals. We used an immunocytochemical method, in combination with cytochrome oxidase histochemistry, to analyze the spatial relationship between neurons that contain neuropeptide Y (NPY) and the CO puffs. Of a total of 606 neurons, only 2.6% of the NPY-containing cells are located in the puffs, whereas the rest are situated in the interpuffs, or at the interface between puffs and interpuffs. The number of NPY-containing neurons in the puffs is substantially less than that expected in an equal volume of the interpuffs (X2 = 13.86; df = 1; P < 0.001).

These observations indicate that columns containing the puffs may differ also from those in the interpuff regions in that they contain a unique array of chemically and morphologically distinct local circuit neurons.

To determine if changes in metabolic capacity revealed by cytochrome oxidase (CO) histochemistry are related to sustained changes in energy-utilizing neuronal activity, we assayed CO levels and recorded multiunit firing rates along nearly tangential penetrations of V1 in seven adult macaque monkeys before and after single, monocular injections of TTX. Within as little as 14 h, TTX blockade began to reduce CO staining in zones of layer 4C that received dominant input from the injected eye. Since simple monocular occlusion has only minor effects on cortical CO levels (Trusk et al., 1990), the changes in activity that were specifically associated with CO depletion were isolated by comparing spike rates during monocular TTX blockade and during monocular occlusion. Five second samples of multiunit spike rate were obtained after 2-min adaptation to each of four adapting fields: black, gray, white, and textured. Results were similar for these four conditions. In layer 4C, ocular dominance zones with input from the TTX eye had ongoing spike rates that were 48% of the rates in zones with input from a normal but occluded eye. In six animals, it was possible to record activity at a single site before, during, and after the onset of TTX blockade. Background activity at these interpuff sites decreased as much as 3-fold in less than 1 h but stabilized within 3–4 h to an average of 53% of pre-TTX rates. These data support the interpretation that energy utilization linked to sustained spike rates partially regulates CO levels under normal conditions, at least in layer 4. Furthermore, changes in neuronal activity induced by retinal TTX preceded the detectable reduction in CO activity in V1 suggesting that the adjustment of CO levels was in response to the altered activity.

The two main receptor subtypes for 5-hydroxytryptamine (5HT) were measured and localized in visual cortical areas of macaque monkey. [3H]5HT was used to label all 5HT-1 receptor subtypes and [3H]ketanserin was used to label 5HT-2 receptors. Both receptor types could be demonstrated in membranes prepared from macaque primary visual cortex. The specificity of these ligands for 5HT-1 or 5HT-2 receptors was demonstrated by the pharmacological profile of inhibitors of the specific binding. 5HT-1A receptor sites were detected by displacement experiments and by direct labeling with [3H]8-hydroxy-2(di-n-propylamino) tetralin 8OH-DPAT. Receptor autoradiography showed that the distribution of these receptor subtypes varied from one part of visual cortex to another. 5HT-1 receptors, labeled with [3H]5HT were present in several bands through layer IV of primary visual cortex with the densest band seen in and above layer IVA: another band was in lower layer VI. The band in layer VI was predominantly 5HT-1A sites. There were two main bands of 5HT-2 receptor sites, the most prominent around the IV/V boundary, and the other extending from layer IVA upwards. Adjacent areas showed 5HT receptors in a broad band corresponding to layer IV. 5HT-1A sites were found in superficial layers of adjacent areas, except V2. These layering patterns did not correspond precisely with cytoarchitectonic layering, nor with the pattern of 5HT-containing presynaptic fibres in published reports. It is important, therefore, in considering the role of the 5HT-containing neurons in cortical function to take account not only of the anatomy of the presynaptic terminals, but also of the postsynaptic receptors upon which the released transmitter will act, and their location within the cortex.

The effect of experimental strabismus on the development of vernier acuity and grating acuity was studied in Macaca nemestrina monkeys. Six monkeys were studied longitudinally beginning near 10 days after birth. Four of the six monkeys developed amblyopia. As is true for human strabismic amblyopes, the deficit in vernier acuity was larger than the deficit in grating acuity in the amblyopic monkeys. The developmental data reveal that this differential disruption of vernier acuity can be understood as a result of a slowed developmental process associated with amblyopia.

The projection from striate and prestriate visual cortex to the pontine nuclei has been studied in the macaque monkey by means of anterograde tracer techniques in order to assess the contribution of anatomically and functionally distinct visual cortical areas to the cortico-ponto-cerebellar loop. No projection to the pons was found from central or paracentral visual-field representations of V1 (striate cortex) or prestriate visual areas V2, and V4. Small patches of terminal labeling occurred after injections of tracer into more peripheral parts of V1, V2 and V3, and into V3A. The terminal fields were located most dorsolaterally in the anterior to middle third of the pons and were quite restricted in their rostro-caudal extent. Injections of V5, however, yielded substantial terminal labeling, stretching longitudinally throughout almost the entire pons. This projection could be demonstrated to arise from parts of V5 receiving input from central visual-field representations of striate cortex, whereas parts of V4 receiving similarly central visual-field input had no detectable projection to the pons. Its distribution may overlap to a large extent with the termination of tecto-pontine fibers and with the termination of fibers from visual areas in the medial bank (area V6 or P0) and lateral bank (area LIP) of the intraparietal sulcus, as well as from frontal eye fields (FEF). It appears that the main information relayed to the cerebellum by the visual corticopontine projection is related to movement in the field of view.

Ibotenic-acid lesions of the magnocelluar portion of the macaque lateral geniculate nucleus were used to examine the role of the M-cell pathway in spatio-temporal contrast sensitivity. A lesion was place in layer 1 of the lateral geniculate of each of two monkeys. Physiological mapping in one animal demonstrated that the visual-field locus of the lesion was on the horizontal meridian, approximately 6 deg in the temporal field. Visual thresholds were tested monocularly in the contralateral eye, and fixation locus was monitored with a scleral search coil to control the retinal location of the test target.

Three threshold measures were clearly disrupted by the magnocellular lesions. Contrast sensitivity for a 1 cycle/deg grating that drifted at 10 Hz was reduced from about twofold greater than, to about the same as, that for 10-Hz counterphase modulated gratings. Sensitivity for a very low spatial frequency (Gaussian blob), 10-Hz flickering stimulus was reduced so severely that no threshold could be measured. In addition, flicker resolution was greatly reduced at lower modulation depths (0.22), but not at higher depths (1.0). Two of the measured thresholds were unaffected by the lesions. Contrast sensitivity for 2 cycle/deg stationary gratings remained intact, and little or no effect on sensitivity was found for 1 cycle/deg, 10-Hz counterphase modulated gratings.

Together, these results suggest that the magnocellular pathway makes little contribution to visual sensitivity at low to moderate temporal frequencies. On the other hand, some contribution to detection sensitivity is evident at lower spatial and high temporal frequencies, especially for drifting stimuli. It appears that a major role of the magnocellular pathway may be to provide input to cortical mechanisms sensitive to rapid visual motion.

Although no visual inputs arise from the blind spot, the same visual attribute there as in the visual field surrounding the blind spot is perceived. Because of this remarkable “perceptual filling-in,” a hole corresponding to the blind spot is not perceived, even when one eye is closed. Does the same phenomenon occur in the case of a scotoma in which visual inputs are lost postnatally due to a retinal lesion? We report that it did: in the macaque monkey, behavioral evidence for filling-in at a scotoma produced by a laser-induced monocular retinal lesion was obtained. The visual receptive fields of neurons in the primary visual cortex (VI) in and around the representation of the visual field corresponding to the scotoma were also mapped, and no clear difference between the retinotopic organization of this part in VI and that found in the normal visual field was found. Also, perceptual filling-in was found to occur only two days after the lesion. These findings suggest that the normal visual system possesses a mechanism that yields filling-in when some part of the retina is damaged, and that such a mechanism requires no topographical reorganization in VI.

The developmental time courses for vernier acuity and grating acuity were measured longitudinally in infant Macaca nemestrina monkeys. Behavioral measurements of vernier and grating acuity were made at regular intervals during development. Near birth, grating acuity is relatively more mature than vernier acuity. The proportional rate of vernier acuity development is faster than that for grating acuity. During the course of development, grating acuity improves approximately 15-fold whereas vernier acuity improves about 60-fold. Both visual functions approach adult levels at about the same age, around 40 weeks postnatally. Although grating acuity develops about four times faster in monkeys than in humans, vernier acuity development in monkeys and humans does not appear to reflect the same relationship. Adult levels of vernier acuity for the monkeys are about a factor of 2 poorer than are typically reported for humans. The differential development of vernier acuity and grating acuity does not necessarily reflect development at different levels of the visual system.

The ventral anterior (VA) nucleus of the thalamus is connected with prefrontal and premotor cortices and with the basal ganglia. Although classically associated with motor functions, recent evidence implicates the basal ganglia in cognition and emotion as well. Here, we used two complementary approaches to investigate whether the VA is a key link for pathways underlying cognitive and emotional processes through prefrontal cortices and the basal ganglia. After application of bidirectional tracers in functionally distinct lateral, medial, and orbitofrontal cortices, we found that projection neurons were embedded in much larger patches of axonal terminations found in the magnocellular part of VA (VAmc), and in the principal part of VA. Connections from medial prefrontal cortices occupied the dorsomedial and ventromedial VA, and orbitofrontal connections were found in ventrolateral VAmc. Moreover, about half of all projection neurons in orbitofrontal areas directed to the VA or VAmc were positive for calbindin but not parvalbumin, even though comparable populations of neurons were positive for each marker in the VA. We then applied tracers in VA and investigated simultaneously projections from all prefrontal areas, the internal segment of the globus pallidus (GPi), the substantia nigra reticulata (SNr), and the thalamic reticular nucleus. Projection neurons were most densely distributed in anterior cingulate areas 24 and 32, and dorsolateral areas 9 and 8, innervating the same VA sites that received projections from a large part of GPi and dorsal SNr. Nearly as many projection neurons originated from cortical layer V as from layer VI. There is evidence that cortical layer VI neurons innervate thalamic neurons that project focally to the middle cortical layers, whereas layer V neurons synapse with thalamic neurons projecting widely to cortical layer I. Projections from layer V to the VA may facilitate cortical recruitment for executive functions within a cognitive context through lateral prefrontal areas, and autonomic responses within an emotional context through anterior cingulate areas.

Membrane voltage was recorded in rod photoreceptors in retina isolated from macaque monkey. The size of the single photon response and the magnitude of membrane voltage fluctuations were assessed in dark- and light-adapted retina. The “dark light” rate ID, defined as the rate of spontaneous photopigment isomerizations that would produce a variance equivalent to that of the noise measured in the dark, was calculated after matched filtering. The average value of 0.08 s−1 fell at the higher end of psychophysical estimates of dark light in human observers. In light-adapted rods the photon response decreased in amplitude and duration, and the magnitude of the voltage fluctuations increased with increasing background light intensity. The signal-to-noise ratio (SNR) for single rods was defined as the ratio of the peak amplitude of the photon response to the standard deviation of the noise fluctuations. The signal-to-noise ratio for dark-adapted rods SNRD was about 7. With increasing background intensity I, the SNR fell as SNRD(1 + I/ID)−1/2. This function may account for the increment thresholds measured with small brief test flashes in human psychophysical experiments.

Recurrent projections comprise a universal feature of cerebral organization. Here, we show that the corticofugal projections from the striate cortex (V1) to the lateral geniculate nucleus (LGN) robustly and multiplicatively enhance the responses of parvocellular neurons, stimulated by gratings restricted to the classical receptive field and modulated in luminance, by over two-fold in a contrast-independent manner at all but the lowest contrasts. In the equiluminant plane, wherein stimuli are modulated in chromaticity with luminance held constant, such enhancement is strongly contrast dependent. These projections also robustly enhance the responses of magnocellular neurons but contrast independently only at high contrasts. Thus, these results have broad functional significance at both network and neuronal levels by providing the experimental basis and quantitative constraints for a wide range of models on recurrent projections and the control of contrast gain.

Cells in area V1 of the anesthetized macaque monkey were stimulated with large texture patterns composed of homogeneous regions of line elements (texels) with different orientations. To human observers, such patterns appear to segregate, with the percept of sharp boundaries between texture regions. Our objective was to investigate whether the boundaries are reflected in the responses of single cells in V1. We measured responses to individual texels at different distances from the texture border. For each cell, patterns of optimally or orthogonally orientated texels were adjusted so that only one texel fell into the receptive field and all other texels fell in the visually unresponsive regions outside. In 37 out of 156 neurons tested (24%), texels immediately adjacent to a texture border evoked reliably larger responses than identical texels farther away from the border. In 17 neurons (11%), responses to texels near the border were relatively reduced. Border enhancement effects were generally stronger than border attenuation effects. When tested with four different border configurations (two global orientations and two edge polarities), many cells showed reliable effects for only one or two configurations, consistent with cells encoding information about the orientation of the texture border or its location with respect to the segmented region. Across the sample, enhancement effects were similar for all texture borders. Modulation by the texture surround was predominantly suppressive; even the responses near texture borders were smaller than those to a single line. We compared these results with the results of a popout test in which the line in the receptive field was surrounded by homogeneous texture fields either orthogonal or parallel to the center line. The patterns of response modulation and the temporal onset of differential responses were similar in the two tests, suggesting that the two perceptual phenomena are mediated by similar neural mechanisms.

Glycine is a major inhibitory neurotransmitter in the mammalian retina and has been shown to influence the responses of ganglion cells. Midget and parasol ganglion cells serve distinct physiological roles in the primate retina and show differences in their response characteristics to light stimuli. In the present study, we addressed the question of whether the expression of glycine receptors differs in midget and parasol ganglion cells. Ganglion cells in the retinae of marmoset and macaque monkeys were injected with Neurobiotin in a live in vitro retinal whole-mount preparation. Retinal pieces were then processed with an antibody against the α1 subunit of the glycine receptor. Strong punctate immunoreactivity indicative of synaptic localization is present in the ON and OFF sublamina of the inner plexiform layer. Many of the immunoreactive puncta coincide with the dendrites of both midget and parasol ganglion cells. Immunoreactive puncta are present on distal and proximal dendrites of ON and OFF cells. These results suggest that ON and OFF midget and parasol cells do not differ with respect to the distribution of the α1 subunit of the glycine receptor.

We studied the effects of contextual modulation in area V1 of anesthetized macaque monkeys. In 146 cells, responses to a single line over the center of the receptive field were compared with those to full texture patterns in which the center line was surrounded by similar lines at either the same orientation (uniform texture) or the orthogonal orientation (orientation contrast). On average, the responses to single lines were reduced by 42% when texture was presented in the surround. Uniform textures often produced stronger suppression (7% more, on average) so that lines with orientation contrast on average evoked larger responses than lines in uniform texture fields. This difference is correlated with perceptual differences between such stimuli, suggesting that physiological mechanisms contributing to the saliency (“popout”) of textural stimuli operate, at least to some degree, even under anesthesia. Significant response modulation by the texture surround was seen in 112 cells (77%). Fifty-three cells (36%) responded differently to the two texture patterns; response preferences for orientation contrast (35 cells; 24%) were seen more often than preferences for uniform textures (18 cells; 12%). The remaining 59 cells (40%) were similarly suppressed by both texture surrounds. Detailed analysis of texture modulation revealed two major components of surround effects: (1) fast nonspecific (“general”) suppression that occurred at about the same latency as excitatory responses and was found in all layers of striate cortex; and (2) differential response modulation that began about 60–70 ms after stimulus onset (about 15–20 ms after the onset of the excitatory response) and was less homogeneously distributed over cortical layers.

Pyramidal neurons in superficial layers of cerebral cortex have extensive horizontal axons that provide a substrate for lateral interactions across cortical columns. These connections are believed to link functionally similar regions, as suggested by the observation that cytochrome-oxidase blobs in the monkey primary visual cortex (V1) are preferentially connected to blobs and interblobs to interblobs. To better understand the precise relationship between horizontal connections and blobs, we intracellularly labeled 20 layer 2/3 pyramidal neurons in tangential living brain slices from V1 of macaque monkeys. The locations of each cell body and the cell's synaptic boutons relative to blobs were quantitatively analyzed. We found evidence for two cell types located at characteristic distances from blob centers: (1) neurons lacking long-distance, clustered axons (somata 130–200 μm from blob centers) and (2) cells with clustered, long-distance axon collaterals (somata <130 μm or >200 μm from blob centers). For all cells, synaptic boutons close to the cell body were located at similar distances from blob centers as the cell body. The majority of boutons from cells lacking distal axon clusters were close to their cell bodies. Cells located more than 200 μm from blob centers were in interblobs and had long-distance clustered axon collaterals selectively targeting distant interblob regions. Cells located less than 130 μm from blob centers were found within both blobs and interblobs, but many were close to traditionally defined borders. The distant synaptic boutons from these cells were generally located relatively near to blob centers, but the neurons closest to blob centers had synaptic boutons closer to blob centers than those farther away. There was not a sharp transition that would suggest specificity for blobs and interblobs as discrete, binary entities. Instead they appear to be extremes along a continuum. These observations have important implications for the function of lateral interactions within V1.