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How cortical neurons process multiple inputs is a fundamental issue in modern neuroscience. Neurons in visual cortical area V1 have been shown to exhibit cross-orientation suppression, where the response to an optimally oriented visual stimulus is reduced by the simultaneous presence of an orthogonally oriented stimulus. This is consistent with the view that cortical neurons respond to multiple inputs with a weighted average (or normalization) of the responses to the inputs presented separately. However, most of these studies have used drifting or counterphase-modulated grating stimuli, potentially confounding orientation effects with non-orientation-specific gain control mechanisms. Additionally, primate vision depends to a great extent on transient stimulus presentations during fixations between saccades. Therefore this study examined the responses of primate V1 neurons to orthogonal flashed-onset single edges and lines, and to their combinations. Single edges or lines do not typically cause strong suppression of the responses to an orthogonal stimulus, even though a grating does. This appears to hold true regardless of the relative contrasts of the orthogonal single lines or edges. This is consistent with response suppression from an orthogonal grating being due to non-orientation-specific contrast gain control (Koeling M, Shapley R, Shelley M. J Comp Neurosci 25: 390–400, 2008; Priebe NJ, Ferster D. Nat Neurosci 9: 552–561, 2006; Walker GA, Ohzawa I, Freeman RD. J.Neurophysiol 79: 227–239, 1998). While normalization mechanisms are clearly important for the cerebral cortex, under many conditions the responses of V1 cortical neurons to an optimally oriented stimulus can be unaffected by the presence of orthogonal stimuli, which may be important to avoid confounding the interpretation of a neural response.

The transformation of spatial (SF) and temporal frequency (TF) tuning functions from broad-band/low-pass to narrow band-pass profiles is one of the key emergent properties of neurons in the mammalian primary visual cortex (V1). The mechanisms underlying such transformation are still a matter of ongoing debate. With the aim of providing comparative insights into the issue, we analyzed various aspects of the spatiotemporal tuning dynamics of neurons in the visual wulst of four awake owls. The wulst is the avian telencephalic target of the retinothalamofugal pathway and, in owls, bears striking functional analogy with V1. Most neurons in our sample exhibited fast and large-magnitude adaptation to the visual stimuli with response latencies very similar to those reported for V1. Moreover, latency increased as a function of stimulus SF but not TF, which suggests that parvo- and magno-like geniculate inputs could be converging onto single wulst neurons. No net shifts in preferred SF or TF were observed along the initial second of stimulation, but bandwidth decreased roughly during the first 200 ms after response latency for both stimulus dimensions. For SF, this occurred exclusively as a consequence of low-frequency suppression, whereas suppression was observed both at the low- and high-frequency limbs of TF tuning curves. Overall these results indicate that SF and TF tuning curves in the wulst are shaped by both feedforward and intratelencephalic suppressive mechanisms, similarly to what seems to be the case in the mammalian striate cortex.

It is well known that electrical activation of striate cortex (area V1) can disrupt visual behavior. Based on this knowledge, we discovered that electrical microstimulation of V1 in macaque monkeys delays saccadic eye movements when made to visual targets located in the receptive field of the stimulated neurons. This review discusses the following issues. First, the parameters that affect the delay of saccades by microstimulation of V1 are reviewed. Second, the excitability properties of the V1 elements mediating the delay are discussed. Third, the properties that determine the size and shape of the region of visual space affected by stimulation of V1 are described. This region is called a delay field. Fourth, whether the delay effect is mainly due to a disruption of the visual signal transmitted through V1 or whether it is a disturbance of the motor signal transmitted between V1 and the brain stem saccade generator is investigated. Fifth, the properties of delay fields are used to estimate the number of elements activated directly by electrical microstimulation of macaque V1. Sixth, these properties are used to make inferences about the characteristics of visual percepts induced by such stimulation. Seventh, the disruptive effects of V1 stimulation in monkeys and humans are compared. Eighth, a cortical mechanism to account for the disruptive effects of V1 stimulation is proposed. Finally, these effects are related to normal vision.

The response of a neuron in striate cortex to an optimally oriented stimulus is suppressed by a superimposed orthogonal stimulus. The neural mechanism underlying this cross-orientation suppression (COS) may arise from intracortical or subcortical processes or from both. Recent studies of the temporal frequency and adaptation properties of COS suggest that depression at thalamo-cortical synapses may be the principal mechanism. To examine the possible role of synaptic depression in relation to COS, we measured the recovery time course of COS. We find it too rapid to be explained by synaptic depression. We also studied potential subcortical processes by measuring single cell contrast response functions for a population of LGN neurons. In general, contrast saturation is a consistent property of LGN neurons. Combined with rectifying nonlinearities in the LGN and spike threshold nonlinearities in visual cortex, contrast saturation in the LGN can account for most of the COS that is observed in the visual cortex.

Various properties of external scenes are integrated during the transmission of information along central visual pathways. One basic property concerns the sensitivity to direction of a moving stimulus. This direction selectivity (DS) is a fundamental response characteristic of neurons in the visual cortex. We have conducted a neurophysiological study of cells in the visual cortex to determine how DS is affected by changes in stimulus contrast. Previous work shows that a neuron integration time is increased at low contrasts, causing temporal changes of response properties. This leads to the prediction that DS should change with stimulus contrast. However, the change could be in a counterintuitive direction, i.e., DS could increase with reduced contrast. This possibility is of intrinsic interest but it is also of potential relevance to recent behavioral work in which human subjects exhibit increased DS as contrast is reduced. Our neurophysiological results are consistent with this finding, i.e., the degree of DS of cortical neurons is inversely related to stimulus contrast. Temporal phase differences of inputs to cortical cells may account for this result.

On the one hand, contrast signals provide information about surface properties, such as reflectance, and patchy illumination conditions, such as shadows. On the other hand, processing of luminance signals may provide information about global light levels, such as the difference between sunny and cloudy days. We devised models of contrast and luminance processing, using principles of logarithmic signal coding and half-wave rectification. We fit each model to individual response profiles obtained from 67 surface-responsive macaque V1 neurons in a center-surround paradigm similar to those used in human psychophysical studies. The most general forms of the luminance and contrast models explained, on average, 73 and 87% of the response variance over the sample population, respectively. We used a statistical technique, known as Akaike's information criterion, to quantify goodness of fit relative to number of model parameters, giving the relative probability of each model being correct. Luminance models, having fewer parameters than contrast models, performed substantially better in the vast majority of neurons, whereas contrast models performed similarly well in only a small minority of neurons. These results suggest that the processing of local and mean scene luminance predominates over contrast integration in surface-responsive neurons of the primary visual cortex. The sluggish dynamics of luminance-related cortical activity may provide a neural basis for the recent psychophysical demonstration that luminance information dominates brightness perception at low temporal frequencies.

Macaques indicated their detection of onset or alteration of 0.2-ms pulses applied in various configurations through electrodes implanted in striate cortex. When microelectrodes were introduced and left in place, the threshold for detection of 100-Hz pulses nearly doubled within 24 h. However, for chronically implanted platinum-alloy macroelectrodes detection thresholds usually remained stable for many months, independently of location within striate cortex or its immediately subjacent white matter. Thresholds were unaffected by the visual conditions, such as light versus darkness, or movement of the eyes; but in one animal blind after acute glaucoma thresholds for loci in striate cortex were permanently decreased by about 50%. Learning to respond to electrical stimulation of the optic tract produced no tendency to respond to such stimulation of striate cortex. Onset of stimulation at a given locus could be detected even in the face of continuous supraliminal stimulation at four surrounding loci on a 3-mm radius. The surround stimulation did alter the threshold of the central locus, but such stimuli could not summate if they were subliminal by some 10%. Cessation of stimulation that had been continuing for 1 min to 1 h could be detected if it were being applied at a level 20–75% above that needed for detection of stimulus onset. Continuous stimulation had a pronounced “priming” effect, in that modulation of frequency or intensity of such stimulation by as little as 5% could be detected (e.g., 20 μA in a background of 500 μA, or

We located clusters of color-selective neurons in macaque striate cortex, as mapped with optical imaging and confirmed with electrophysiological recordings. By comparing responses to an equiluminant red/green stimulus versus a high-contrast luminance stimulus, we were able to reveal a patchy distribution of color selectivity. Other color imaging protocols, when compared with electrophysiological data, did not reliably indicate the location of functional structures. The imaged color patches were compared with other known functional subdivisions of striate cortex. There was a high degree of overlap of the color patches with the cytochrome-oxidase (CO) blobs. The patches were often larger than a single blob in size, however, and in some instances spanned two neighboring blobs. More than one-half (56%) of the color-selective patches seen in optical imaging were not confined to one ocular dominance (OD) column. Almost one-quarter of color patches (23%) extended across OD columns to encompass two blobs of different eye preference. We also compared optical images of orientation selectivity to maps of color selectivity. Results indicate that the layout of orientation and color selectivity are not directly related. Specifically, despite having similar scales and distributions, the maps of orientation and color selectivity were not in consistent alignment or registration. Further, we find that the maps of color selectivity and of orientation are each only loosely related to maps of OD. This description stands in contrast to a common depiction of color-selective regions as identical to CO blobs, appearing as pegs in the centers of OD columns in the classical “ice cube” model. These results concerning the pattern of color selectivity in V1 support the view (put forth in previous imaging studies of the organization of orientation and ocular dominance) that there is not a fundamental registration of functional hypercolumns in V1.

The optic disk is a region of the retina consisting mainly of ganglion cell axons and blood vessels, which generates a visual scotoma known as the blind spot (BS). Information present in the surroundings of the BS can be used to complete the missing information. However, the neuronal mechanisms underlying these perceptual phenomena are poorly understood. We investigate the topography of the BS representation (BSR) in cortical area V1 of the capuchin monkey, using single and multiple electrodes. Receptive fields (RFs) of neurons inside the BSR were investigated using two distinct automatic bias-free mapping methods. The first method (local mapping) consisted of randomly flashing small white squares. For the second mapping method (global mapping), we used a single long bar that moved in one of eight directions. The latter stimulus was capable of eliciting neuronal activity inside the BSR, possibly attributable to long-range surround activity taking place outside the borders of the BSR. Importantly, we found that the neuronal activity inside the BSR is organized topographically in a manner similar to that found in other portions of V1. On average, the RFs inside the BS were larger than those outside. However, no differences in orientation or direction tuning were found between the two regions. We propose that area V1 exhibits a continuous functional topographic map, which is not interrupted in the BSR, as expected by the distribution of photoreceptors in the retina. Thus V1 topography is better described as “visuotopic” rather than as a discontinuous “retinotopic” map.

Snider, R. K., J. F. Kabara, B. R. Roig, and A. B. Bonds. Burst firing and modulation of functional connectivity in cat striate cortex. J. Neurophysiol. 80: 730–744, 1998. We studied the influences of the temporal firing patterns of presynaptic cat visual cortical cells on spike generation by postsynaptic cells. Multiunit recordings were dissected into the activity of individual neurons within the recorded group. Cross-correlation analysis was then used to identify directly coupled neuron pairs. The 22 multiunit groups recorded typically showed activity from two to six neurons, each containing between 1 and 15 neuron pairs. From a total of 241 neuron pairs, 91 (38%) had a shifted cross-correlation peak, which indicated a possible direct connection. Only two multiunit groups contained no shifted peaks. Burst activity, defined by groups of two or more spikes with intervals of ≤8 ms from any single neuron, was analyzed in terms of its effectiveness in eliciting a spike from a second, driven neuron. We defined effectiveness as the percentage of spikes from the driving neuron that are time related to spikes of the driven neuron. The effectiveness of bursts (of any length) in eliciting a time-related response spike averaged 18.53% across all measurements as compared with the effectiveness of single spikes, which averaged 9.53%. Longer bursts were more effective than shorter ones. Effectiveness was reduced with spatially nonoptimal, as opposed to optimal, stimuli. The effectiveness of both bursts and single spikes decreased by the same amount across measurements with nonoptimal orientations, spatial frequencies and contrasts. At similar firing rates and burst lengths, the decrease was more pronounced for nonoptimal orientations than for lower contrasts, suggesting the existence of a mechanism that reduces effectiveness at nonoptimal orientations. These results support the hypothesis that neural information can be emphasized via instantaneous rate coding that is not preserved over long intervals or over trials. This is consistent with the integrate and fire model, where bursts participate in temporal integration.

Smith, Earl L., III, Yuzo M. Chino, Jinren Ni, William H. Ridder III, and M.L.J. Crawford. Binocular spatial phase tuning characteristics of neurons in the macaque striate cortex. J. Neurophysiol. 78: 351–365, 1997. We employed microelectrode recording techniques to study the sensitivity of individual neurons in the striate cortex of anesthetized and paralyzed monkeys to relative interocular image disparities and to determine the effects of basic stimulus parameters on these cortical binocular interactions. The visual stimuli were drifting sine wave gratings. After the optimal stimulus orientation, spatial frequency, and direction of stimulus movement were found, the cells' disparity tuning characteristics were determined by measuring responses as a function of the relative interocular spatial phase of dichoptic grating pairs. No attempts were made to assess absolute position disparities or horizontal disparities relative to the horopter. The majority (∼70%) of simple cells were highly sensitive to interocular spatial phase disparities, particularly neurons with balanced ocular dominances. Simple cells typically demonstrated binocular facilitation at the optimal phase disparity and binocular suppression for disparities 180° away. Fewer complex cells were phase selective (∼40%); however, the range of disparity selectivity in phase-sensitive complex cells was comparable with that for simple cells. Binocular interactions in non-phase-sensitive complex cells were evidenced by binocular response amplitudes that differed from responses to monocular stimulation. The degree of disparity tuning was independent of a cell's optimal orientation or the degree of direction tuning. However, disparity-sensitive cells tended to have narrow orientation tuning functions and the degree of disparity tuning was greatest for the optimal stimulus orientations. Rotating the stimulus for one eye 90° from the optimal orientation usually eliminated binocular interactions. The effects of phase disparities on the binocular response amplitude were also greatest at the optimal spatial frequency. Thus a cell's sensitivity to absolute position disparities reflects its spatial tuning characteristics, with cells sensitive to high spatial frequencies being capable of signaling very small changes in image disparity. On the other hand, stimulus contrast had relatively little effect on a cell's disparity tuning, because response saturation occurred at the same contrast level for all relative interocular phase disparities. Thus, as with orientation tuning, a cell's optimal disparity and the degree of disparity selectivity were invariant with contrast. Overall, the results show that sensitivity to interocular spatial phase disparities is a common property of striate neurons. A cell's disparity tuning characteristics appear to largely reflect its monocular receptive field properties and the interocular balance between excitatory and inhibitory inputs. However, distinct functional classes of cortical neurons could not be discriminated on the basis of disparity sensitivity alone.

1. Neurons that are selectively sensitive to the direction of motion of elongated contours have been found in several cortical areas in many species. However, in the striate cortex of the cat and monkey, and the extrastriate posteromedial lateral suprasylvian visual area of the cat, such cells are generally component motion selective, signaling only the direction of movement orthogonal to the preferred orientation; a direction that is not necessarily the same as the motion of the entire pattern or texture of which the cell's preferred contour is part. The primate extrastriate middle temporal area is the only cortical region currently known to contain a substantial population of pattern-motion-selective cells that respond to the shared vector of motion of mixtures of contours. 2. From analyzing published data on the connectivity of the cat's cortex, we predicted that the anterior ectosylvian visual area (AEV), situated within the anterior ectosylvian sulcus, might be a higher-order motion processing area and thus likely to contain pattern-motion-selective neurons. This paper presents the results of a study on neuronal responses in AEV. 3. Ninety percent of AEV cells that responded strongly to drifting grating and/or plaid stimuli were directionally selective (directionality index > 0.5). For this group, the mean directionality index was 0.75. Moreover, 55% of these cells were unequivocally classified as pattern motion selective and only one neuron was classified as definitely component motion selective. Thus high-level pattern motion coding occurs in the cat extrastriate cortex and is not limited to the primate middle temporal area. 4. AEV contains a heterogeneous population of directionally selective cells. There was no clear relation between the degree of directional selectivity for plaids or gratings and the degree of selectivity for pattern motion or component motion. Nevertheless, 28% of the highly responsive cells were both more strongly modulated by plaids than gratings and more pattern motion selective than component motion selective. Such cells could correspond to a population of "selection units" signaling the salience of local motion information. 5. AEV lacks global retinotopic order but the preferred direction of motion of neurons (rather than axis of motion, as in the middle temporal area and the posteromedial lateral suprasylvian visual area) is mapped systematically across the cortex. Our data are compatible with AEV being a nonretinotopic, feature-mapped area in which cells representing similar parts of "motion space" are brought together on the cortical sheet.

1. We recorded the responses of 37 striate cortical complex cells in fixating monkeys while presenting a set of oriented stimuli that varied in contrast. 2. The two response parameters of strength and latency can be interpreted as a code: the strength defines the stimulus form (here the orientation), and the latency is more a function of the stimulus contrast. 3. Synchronization based on latency could make a strong contribution to the process of organizing the neural responses to different objects, i.e., binding.

1. In alert macaque monkeys, multiunit activity is encountered in an alternating sequence of silent and spontaneously active zones as an electrode is lowered through the striate cortex (V1). 2. Individual neurons that are spontaneously active in the dark usually have a maintained discharge in the light. Because both types of discharge occur in the absence of deliberate stimulation, we call them the "ongoing" activity. The zones with ongoing activity correspond to the cytochrome oxidase (CytOx)-rich geniculorecipient layers 4A, 4C, and 6, whereas the adjacent layers 2/3, 4B, and 5 have little ongoing activity. 3. The widths of receptive field activating regions (ARs) are positively correlated with the cells' ongoing activity. Cells with larger ARs are preferentially located in the CytOx-rich (input) layers, and many are unselective for stimulus orientation. However, approximately 90% of the cells in the silent layers are orientation selective, and they often have small ARs. 4. The laminar distribution of selectivity for orientation and direction of movement in alert animals is consistent with earlier results from anesthetized animals, but the laminar distribution of AR widths differs. In alert macaques, the ARs of direction-selective cells in layer 4B and of orientation-selective cells in layer 5 are among the smallest in V1. 5. Our findings indicate that the input layers of V1 (4A, 4C, and 6) have a diversity of AR widths, including large ones. Cortical processing produces receptive fields in some of the output layers (4B and 5) that are restricted to small ARs with high resolution of spatial position. These results imply potent lateral and/or interlaminar interactions in alert animals in early cortical processing. The diversity of AR widths generated in V1 may contribute to detection of fine detail in the presence of contrasting backgrounds--the early stages of figure-ground discrimination.

1. Whether complex (C) cells are the only truly texture-sensitive units in the cat's primary visual cortex remains controversial. In view of the strong physiological significance of having putatively only one class of cells sensitive to visual noise in the striate cortex, we reinvestigated this issue. Sensitivities of simple (S) and C cells to noise were quantitatively studied and compared in order to clearly document the response properties of cells in the striate cortex to visual noise and to establish whether one can unequivocally segregate S from C cells on the basis of those specific properties. 2. Receptive fields were stimulated with all relevant stimuli, i.e., drifting sine-wave gratings, electronically generated noise pattern of 256 x 256 elements (ratio 1:1 of dark and light elements), and flashing and moving bars (both bright and dark). 3. A total of 60 S cells out of 85 (70.6%) and 90 C cells out of 101 (81.8%) responded to the motion of visual noise. Responses of most C cells were sustained, i.e., their discharge rate was maintained at a constant level throughout presentation of the stimulus. On the other hand, responses of the majority of S cells were characterized by several bursts of discharges. On average, optimal firing rates were greater for gratings than for noise. 4. For practically all cells, responses to noise varied as a function of direction of motion. The mean direction bandwidths were, respectively, 43 +/- 24 degrees and 48 +/- 23 degrees (mean +/- SD) for S and C cells. In both groups, neurons were more broadly tuned for the direction of noise than that of gratings (t-test, P < 0.001). We rarely observed bimodal tuning curves for noise, with each peak lying on either side of the orientation curve. These results could be expected if one considers texture stimuli not in the space domain (as dot patterns) but in the frequency domain, i.e., patterns containing all spatial frequencies and orientations. 5. In general, the direction indexes of S and C cells were similar whether they were stimulated by drifting noise or gratings. S cells had a slight tendency to be more direction selective for noise than for gratings. 6. For all S and C cells tested, responses to noise varied as a function of drift velocity. The mean optimal velocity was 12.9 and 10.2 degrees/s for S and C cells, respectively (t-test, P > 0.05). Most cells were band-pass with mean bandwidths of 2.2 and 2.7 octaves for S and C cells, respectively.(ABSTRACT TRUNCATED AT 400 WORDS)

This essay looks at the historical significance of two APS classic papers that are freely available online: Wurtz RH. Visual receptive fields of striate cortex neurons in awake monkeys. J Neurophysiol 32: 727–742, 1969 ( http://jn.physiology.org/cgi/reprint/32/5/727 ). Wurtz RH. Comparison of effects of eye movements and stimulus movements on striate cortex neurons of the monkey. J Neurophysiol 32: 987–994, 1969 ( http://jn.physiology.org/cgi/reprint/32/6/987 ).

Macaques were trained to signal their detection of electrical stimulation applied by a movable microelectrode to perifoveal striate cortex. Trains of ≤100 cathodal, 0.2-ms, constant current pulses were delivered at 50 or 100 Hz. The minimum current that could be reliably detected was measured at successive depths along radial electrode penetrations through the cortex. The lowest detection thresholds were routinely encountered when the stimulation was applied to layer 3, particularly just at the juncture between layers 3 and 4A. On the average, there was a twofold variation in threshold along the penetrations, with the highest intracortical thresholds being in layers 4C and 6. Variations as high as 20-fold were obtained in some individual penetrations, whereas relatively little change was observed in others. The minimum detectable current was 1 μA at a site in layer 3, i.e., 10–100 times lower than that for surface stimulation. Because macaques, as do human subjects, find electrical stimulation of striate cortex to be highly similar at all loci (a phosphene in the human case), it is puzzling as to how such uniformity of effect evolves from the exceedingly intricate circuitry available to the effective stimuli. It is hypothesized that the stimulus captures the most excitable elements, which then suppress other functional moieties, producing only the luminance of the phosphene. Lowest thresholds presumably are encountered when the electrode lies among these excitable elements that can, with higher currents, be stimulated directly from some distance or indirectly by the horizontal bands of myelinated axons, the stria of Baillarger.

We have shown in the accompanying paper that optical imaging of macaque striate cortex reveals patches that are preferentially activated by equiluminant chromatic gratings compared with luminance gratings. These imaged color patches are highly correlated, although not always in one-to-one correspondence, with the cytochrome-oxidase (CO) blobs. In the present study, we have investigated the electrophysiological properties of neurons in the imaged color patches and the CO blobs. Our results indicate that individual blobs tend to contain cells of only one type of color opponency: either red/green or blue/yellow. Individual imaged color patches, however, can bridge blobs of similar opponency or differing opponency. When imaged color patches contain two blobs of differing opponency, the cells in the bridge region exhibit mixed color properties that are not opponent along the two cardinal color axes (either red/green or blue/yellow). Two blobs within a single imaged color patch receive input from the same eye or from different eyes. In the latter case, the bridge region between blobs contains binocular cells that are color selective. Because the cells recorded in imaged color patches were more color selective and unoriented than cells outside of color patches, color properties appear to be organized in a clustered and segregated fashion in primate V1.

In cortical simple cells of cat striate cortex, the response to a visual stimulus of the preferred orientation is partially suppressed by simultaneous presentation of a stimulus at the orthogonal orientation, an effect known as “cross-orientation inhibition.” It has been argued that this is due to the presence of inhibitory connections between cells tuned for different orientations, but intracellular studies suggest that simple cells receive inhibitory input primarily from cells with similar orientation tuning. Furthermore, response suppression can be elicited by a variety of nonpreferred stimuli at all orientations. Here we study a model circuit that was presented previously to address many aspects of simple cell orientation tuning, which is based on local intracortical connectivity between cells of similar orientation tuning. We show that this model circuit can account for many aspects of cross-orientation inhibition and, more generally, of response suppression by nonpreferred stimuli and of other nonlinear properties of responses to stimulation with multiple gratings.

1. Monkeys with large unilateral surgical ablations of striate cortex, sustained either in adulthood or at 5–6 wk of age, were trained on an oculomotor detection and localization task and tested with visual stimuli in the hemifields ipsilateral and contralateral to the lesion 2–5 yr after surgery. 2. Monkeys with lesions sustained in adulthood were largely unable to detect stimuli in the hemifield contralateral to the lesion, with only one monkey showing recovery toward the end of testing. Monkeys with lesions of striate cortex made in infancy, however, each showed residual detection capacity at the beginning of testing and improved to near normal by the end of testing. 3. Each of the monkeys showing a residual ability to detect within the contralateral hemifield was also able to localize visual targets with eye movements. 4. These findings demonstrate that the vision surviving striate cortex damage in primates is more robust after early damage as has been shown to be the case for primary somatosensory, motor, and association cortex.

1. This work explores a mechanism that the brain may use for linking related percepts. It has been proposed that temporal relationships in the firing of neurons may be important in indicating how the stimuli that activate those neurons are related in the external world. Such temporal relationships cannot be seen with conventional receptive field mapping but require cross-correlation and auto-correlation analysis. 2. In the cat and the macaque monkey, cells with similar receptive field properties show correlated firing even when their receptive fields do not overlap. Here I report that in the squirrel monkey, as in the cat, pairs of cells < or = 5 mm apart can show correlated firing, and these correlations between pairs of cells are often stronger when they are stimulated by a single contour. This suggests that the correlations reflect not only permanent connections between cells with similar receptive fields, but in addition may encode information that the activating stimuli are continuous or part of a single object. I also find that, as in the cat, and contrary to some other reports on experiments in monkeys, the correlated firing is often rhythmic. These recordings further indicate that periods of rhythmicity are associated with stronger interneuronal synchrony, which is consistent with the hypothesis that recurrent feedback loops are involved in generating both. 3. Pairs of cells in the same cortical column, but at different depths also showed correlated firing, but with several milliseconds difference in timing between layers. This was true for cells at different depths within layer 2/3 and for pairs of cells in different layers (2/3 vs. 4B or 4C alpha), providing evidence for cross-talk between the magno- and parvocellular streams.

1. Responses of simple cells in cat striate cortex were studied with flashed light-slit stimuli. The responses to bars flashed in different positions in the receptive field were assessed quantitatively before and after periods of prolonged stimulation of one small region. This type of prolonged stimulation resulted in reduced responsivity over a limited zone within the simple cell receptive field. 2. The adaptation-induced responsivity decrement was generally confined to the receptive-field subregion that was adapted (either ON or OFF). Prolonged stimulation within an ON region did not usually result in adaptation effects that spread into neighboring OFF regions. Furthermore, the adaptation-induced response decrement did not necessarily spread throughout the subregion in which the adapting stimulus was presented. The adaptation effects from prolonged stimulation at a single receptive-field position spread throughout the subregion in nearly one-half of the 25 cells examined for position-specific adaptation. Another subpopulation of neurons (n = 12) displayed adaptation effects that spread through only one-half of the subregion, whereas in two neurons the spread of the adaptation effect was even more restricted and encompassed only one-fourth of the subregion. 3. The spread of adaptation was not systematically related to the size of the stimulus presented, the size of the receptive field, or the magnitude of the adaptation-induced response decrements but was significantly correlated with the spatial wavelength of the cell (the reciprocal of the cell's preferred spatial frequency) and with the size of the subregion in which the adapting stimulus was presented. Cells with large receptive-field subregions and long wave-lengths showed adaptation effects that spread further than those of cells with small subregions. 4. The adaptation effects from repeated stimulation at a single receptive-field position did not spread symmetrically across the receptive field, and the preferred direction of motion for a given cell indicated the direction of the asymmetric spread of the adaptation. Receptive-field positions that would be stimulated by a light slit originating at the point of adaptation and moving in the preferred direction (preferred side) showed greater adaptation-induced response decrements than did receptive-field positions that would be stimulated by a light slit moving in the opposite direction from the point of adaptation (nonpreferred side). There was significant enhancement of responses at some receptive-field positions on the nonpreferred side of the point of adaptation.(ABSTRACT TRUNCATED AT 400 WORDS)

1. Binocularity and receptive-field type of cortical neurons were assessed relative to the cortical layer in which the neurons were recorded and to receptive-field position in the visual field. 2. Receptive fields were observed up to 2 degrees into the ipsilateral half of the visual field. In the region up to 2 degrees on either side of the vertical meridian, the relative contribution of the ipsilateral eye was reduced. This progression in ocular dominance from ipsilateral to contralateral visual field agrees well with the distribution of X-cells about the nasotemporal division. 3. The region of maximum binocularity in each hemifield was found to be a 12 degree wide vertical strip extending from the vertical meridian to 12 degrees contralateral. In the representation of the central 12 degree strip, most units in all cortical layers were binocular. 4. Low levels of binocularity were observed at a considerable distance before the monocular portion of the visual field was reached. 5. The decrease in binocularity for simple cells occurred closer to the vertical meridian than for complex cells. 6. The proportions of cells classified as simple or complex did not change with position in the visual field. 7. At all locations in the visual field, complex cells showed a higher percentage of binocularity than simple cells. 8. The proportions of two types of simple cells, I and II, and complex cells were variable between cortical layers. Layer IV contained predominantly simple II cells, whereas layer V contained predominantly complex cells. 9. The results are discussed in terms of visual perception and the dynamic pattern of visual stimulation around a moving animal, the optic flow field.

1. The receptive-field properties of corticotectal cells in the monkey's striate cortex were studied using stationary and moving stimuli. These cells were identified by antidromic activation from the superior colliculus. 2. Corticotectal cells form a relatively homogeneous group. They are found primarily in layers 5 and 6. These cells can usually be classified as CX-type cells but show broader orientation tuning, larger receptive fields, higher spontaneous activity, and greater binocular activation than CX-type cells do in general. A third of the corticotectal cells were direction selective. 3. These results suggest that the cortical input to the superior colliculus is not directly responsible for the receptive-field properties of collicular cells. We propose that this input has a gating function in contributing to the control of the downflow of excitation from the superficial to the deep layers of the colliculus.

Simultaneous recordings were made from small collections (2-7) of spontaneously active single units in the striate cortex of unanesthetized cats, by means of chronically implanted electrodes. The recorded spike trains were computer scanned for bursts of spikes, and the bursts were catalogued and studied. The firing rates of the neurons ranged from 0.16 to 32 spikes/s; the mean was 8.9 spikes/s, the standard deviation 7.0 spikes/s. Bursts of spikes were assigned a quantitative measure, termed Poisson surprise (S), defined as the negative logarithm of their probability in a random (Poisson) spike train. Only bursts having S greater than 10, corresponding to an occurrence rate of about 0.01 bursts/1,000 spikes in a random spike train, were considered to be of interest. Bursts having S greater than 10 occurred at a rate of about 5-15 bursts/1,000 spikes, or about 1-5 bursts/min. The rate slightly increased with spike rate; averaging about 2 bursts/min for neurons having 3 spikes/s and about 4.5 bursts/min for neurons having 30 spikes/s. About 21% of the recorded units emitted significantly fewer bursts than the rest (below 1 burst/1,000 spikes). The percentage of these neurons was independent of spike rate. The spike rate during bursts was found to be about 3-6 times the average spike rate; about the same for longer as for shorter bursts. Bursts typically contained 10-50 spikes and lasted 0.5-2.0 s. When the number of spikes in the successively emitted bursts was listed, it was found that in some neurons these numbers were not distributed at random but were clustered around one or more preferred values. In this sense, bursts occasionally "recurred" a few times in a few minutes. The finding suggests that neurons are highly reliable. When bursts of two or more simultaneously recorded neurons were compared, the bursts often appeared to be temporally close, especially between pairs of neurons recorded by the same electrode; but bursts seldom started and ended simultaneously on two channels. Recurring bursts emitted by one neuron were occasionally accompanied by time-locked recurring bursts by other neurons.

1. Eye movements were recorded before and after bilateral occipital lobectomy in six rhesus monkeys trained to fixate and to follow small targets. Striate cortex was completely removed in two animals; small islands islands remained in the others. In all animals portions of extrastriate cortex were also removed but the medial superior temporal area in the superior temporal sulcus was largely spared. Optokinetic nystagmus (OKN) was markedly altered but not abolished in all animals. The immediate pursuit component of OKN was eliminated leading to a poor response to stimuli comprised of high frequencies. The velocity-storage component of OKN was present, but the maximum value of OKN that could be achieved was decreased to 6 and 16 degrees/s in the two most severely affected animals (preop, 65-116 degrees/s). The residual OKN was similar to that of afoveate animals with a diminished response to high velocities of retinal-image motion and a temporal to nasal predominance during monocular viewing. 2. In the initial postoperative period all animals appeared completely blind. Within 1-6 mo, however, they regained an ability to make visually guided saccades to, and smooth pursuit of, small targets. Saccades were nearly as accurate as preoperatively, but saccade amplitudes were more variable and saccade latencies increased. In the two animals with a complete removal of striate cortex, gains (eye velocity/target velocity) of smooth pursuit during sinusoidal tracking (60 degrees/s, 0.5 Hz) were 0.9 and 0.95. During tracking of step-ramp (Rashbass) stimuli with 60 degrees/s ramps, the average acceleration of the eyes during the first 120 ms of smooth pursuit was 189-278 degrees.s-1.s-1 (preop range, 154-418 degrees.s-1.s-1). In other respects, though, smooth pursuit was not normal. Latencies were increased two- to threefold, and tracking was more variable. 3. Paradoxically, as visually guided saccades and pursuit recovered, some other ocular motor functions deteriorated. Spontaneous and gaze-evoked nystagmus developed 3-6 mo after occipital lobectomy; the time constant of the neural eye-position integrator dropped to values as low as 2.6-4.8 s. The maximum slow-phase velocity of OKN also decreased. 4. The findings immediately after occipital lobectomy indicate that in normal primates occipital cortex is necessary for visually guided saccades and smooth pursuit as well as for the immediate component of OKN. Occipital cortex also makes the predominant contribution toward the generation of the velocity-storage component of OKN.(ABSTRACT TRUNCATED AT 400 WORDS)

1. The selectivity of adaptation to unidirectional motion was examined in neurons of the cat striate cortex. Following prolonged stimulation with a unidirectional high-contrast grating, the responsivity of cortical neurons was reduced. In many units this decrease was restricted to the direction of prior stimulation. This selective adaptation produced changes in the degree of direction selectivity of the cortical units (as measured by the ratio of the response to motion in the preferred direction to that in the nonpreferred direction). 2. The initial strength of the directional preference of a given cortical unit did not determine the degree of direction-selective adaptation. Indeed, even non-direction-selective units could exhibit pronounced direction-selective adaptation. The degree of direction-selective adaptation was also independent of the overall decrease in responsivity during adaptation. 3. There was no difference between simple and complex cells in the total amount of adaptation observed. The selectivity of the adaptation, however, did differ between these two cell types. As a group, simple cells showed significant direction-selective adaptation, whereas complex cells did not. The directional preference of most simple cells decreased following preferred direction adaptation and many highly direction selective simple cells became non-direction selective. In addition, simple cells became significantly more direction selective following nonpreferred direction adaptation. 4. Some complex cells also demonstrated direction-selective adaptation. There was, however, much more variability among complex cells than simple cells. Some complex cells actually increased direction selectivity following preferred direction adaptation. These differences between simple and complex cells suggest that changes in direction selectivity following unidirectional adaptation are not due to simple neuronal fatigue of the unit being recorded, but depend on selective adaptation of afferent inputs to the unit. 5. The spontaneous activity of many cortical neurons decreased following preferred direction adaptation but increased following adaptation in the nonpreferred direction. The response to a stationary grating also decreased following preferred direction adaptation. However, there was very little change in the response to a stationary grating following adaptation in the nonpreferred direction.

1. The response properties of single cells in monkey striate cortex were examined using moving bars, square-wave gratings, and sine-wave gratings. 2. The moving of cells studied were not selective for bar width or for the spatial frequency of square-wave gratings. 3. Most cells responded selectively to the spatial frequency of the sine-wave gratings. 4. The spatial frequency of the sine-wave grating eliciting the optimal response could not be predicted from the organization of the receptive field of each cell as determined by stationary or moving stimuli. 5. The sharpness of spatial-frequency selectivity is only slightly more pronounced in S-type cells than in CX-type cells. 6. S-type and CX-type cells differ significantly in the temporal modulation of their discharges to gratings. S-type cells discharge in sharp bursts to each cycle which traverses the receptive field. CX-type cells discharge in a rather continuous fashion. This measure can be used reliably to classify cells as S or CS type.

1. Quantitative analyses of orientation specificity and ocular dominance were carried out in striate cortex of the rhesus monkey. 2. Sharpness of orientation selectivity was greater for simple (S type) than for complex (CX type) cells. CX-type cells became more broadly tuned in the deeper cortical layers: S-type cells were equally well tuned throughout the cortex. 3. Sharpness of orientation selectivity for S-type cells was similar at all retinal eccentricities studied (0 degrees - 20 degrees from the fovea):in CX-type cells orientation selectivity decreased slightly with increasing eccentricity. 4. The orientation tuning of binocular cells was similar when mapped separately through each eye. 5. Orientation selectivity and direction selectivity are independent of each other, suggesting that separate neural mechanisms give rise to them. 6. More CX-type cells can be binocularly activated than S-type cells (88% versus 49%). The ocular dominance of S-type cells is similar in all cortical layers: for CX-type cells there is an increase in the number of cells in ocular-dominance category 4 in layers 5 and 6.

The purposes of this study were 1) to relate the receptive-field characteristics of area 17 cells to their afferent and efferent connections, and 2) to obtain quantitative data from area 17 neurons for later comparison with area 18 cells. Intra- and extracellular recordings were obtained in paralyzed preparations which were anesthetized with nitrous oxide. The connectivities of the recorded cells were determined from responses to electrical stimulation of afferent and efferent pathways. In parallel to the classification of units as simple and complex cells, the receptive fields were grouped in four classes according to the spatial arrangement of on- and off-areas; class I, fields with exclusive on- or off-areas; class II, fields with spatially separate on- and off-areas; class III, fields with mixed on-off areas; class IV, fields which could not be mapped with stationary stimuli. The results from electrical stimulation suggest two major classes of cells: cells in the first group are driven mainly or exclusively by LGN afferents. They rarely receive additional excitation from intrinsic or callosal afferents and rarely possess corticofugal axons. Cells in the second group receive either converging inputs from LGN afferents and further intrinsic afferents or only from intrinsic afferents. They frequently received additional input from callosum and from recurrent collaterals of corticofugal axons. They project subcortically more often than cells in the first group. Cells in both groups can be driven either by X- or Y-type afferents. Cells in the first group have mainly class I and class II fields or simple fields, whereas the neurons in the second group have mainly class III and class IV fields or complex fields. Thus, simple and complex cells differ in their connectivity patterns, but the discriminative parameter is neither the selective connection to the X- or the Y-system nor, in a strict sense, the synaptic distance from subcortical input. From the combined consideration of receptive-field properties and connectivity patterns it is concluded that class I and class II cells or simple cells are concerned mainly with the primary analysis of subcortical activity, whereas class III and class IV cells or complex cells perform a correlative analysis between highly convergent activity from extrinsic and intrinsic afferents.

SUMMARY AND CONCLUSIONS 1. The representation of the visual field in the striate projection zone in the posterior portion of the superior temporal sulcus of the macaque (MT) was mapped with multiunit electrodes. The animals were immobilized and anesthetized and in each animal 25-35 electrode penetrations were typically made over several recording sessions. 2. MT contains a representation of virtually the entire contralateral visual field. The representation of the vertical meridian forms its ventrolateral border and lies near the bottom of the lower bank of the superior temporal sulcus (STS). The representation of the horizontal meridian runs across the floor of STS. The upper field is located ventral and anterior and the lower field dorsal and posterior. The medial border lies at the junction of the floor of STS and its upper bank. 3. MT is similar to striate cortex in being a first-order transformation of the visual field. In both areas, receptive-field size and cortical magnification increase with eccentricity. MT is much smaller than striate cortex and has much larger receptive fields at a given eccentricity and a cruder topography. 4. The results further support the suggestion that MT in the macaque is homologous to visual area MT in New World primates.

1. In the infragranular layers of the striate cortex of three monkeys, we studied tangential neuronal interactions by analyzing cross-correlograms calculated from spike trains recorded with 30 closely spaced microelectrodes. 2. There are two major types of correlogram structures--"narrow" peaks a few milliseconds wide, sometimes accompanied by small lateral troughs, and "broad" peaks approximately 30- to 100-ms wide. Isolated troughs are rare. Both types of structures are superimposed in the same correlograms; they are not due to shared optical stimulation. 3. In layer VI, narrow peaks are largest in a short lateral range of approximately 220 micron, and they depend on ocularity. In layer V, the lateral range is greater, and the dependency on ocularity is weak. 4. In addition, narrow peaks are largest at distances of 160 micron if the angles of preferred orientation are similar. In layer VI, however, at tangential distances of 300-400 micron, peaks are smaller, and troughs are found more often, for neuron pairs with parallel orientations compared with those with orthogonal orientations. From the agreement of this finding with a cooperative theory, we conclude that orientation selectivity is shaped by collective interactions. 5. Broad peaks always depend on ocularity, and the associated lateral interaction range exceeds the maximum of 1 mm investigated. Their size sharply decreases with receptive-field distance. 6. Average mutual delays of spikes of neuron pairs, manifest as lateral displacements of broad peaks, are interdependent; the delay between neurons 1 and 3 is the sum of that of neurons 1 and 2 and of neurons 2 and 3. This feature permits to rank the neurons on a "delay scale." 7. We conclude from 5 and 6 above that broad peaks partly result from intraretinal interactions whose effects are transmitted to the cortex via slow and fast pathways. 8. Lateral troughs adjacent to narrow peaks provide evidence that neurons at the "slow" end of the delay scale inhibit those at the "fast" end, and to a lesser extent, nondirectional neurons inhibit directional ones.

The present study examines the chromatic organization of foveal striate cortex in the awake monkey by means of a series of microelectrode penetrations made as perpendicular as possible to the layers. The study includes 79 penetrations and 261 cells, of which 218 were tested systematically for color selectivity. Detailed analyses are conducted on a subset of 41 penetrations, which included 164 color-tested cells, an average of four cells per penetration. The penetrations were divided into two major categories on the basis of orientation selectivity testing. One group of penetrations contained at least one nonoriented cell in the first 600 microns of microelectrode trajectory (upper layers), whereas the other group of penetrations contained only oriented cells in the first 600 microns of microelectrode trajectory. The two groups were called N (nonoriented) and O (oriented), respectively. Analysis of the color properties of cells in N and O penetrations revealed that middle layer cells in N penetrations showed poor responses to white light, and color preferences for endspectral wavelengths, i.e., red or blue. Middle layer cells in O penetrations, by contrast, responded well to white light and to midspectral wavelengths. There were two subgroups of N penetrations, characterized by predominantly red (NR) or blue (NB) sensitivity in the middle layers. O penetrations could likewise be divided up into three subgroups (OG, OY, OW), characterized, respectively, by predominant sensitivity to greenish wavelengths (490-540 nm), yellowish wavelengths (550–600 nm), or white (i.e., all colors). Despite the identification of five subgroups, similarities between NR and OY, between NB and OG, and between OY and OW subgroups might be consistent with a continuum. The middle layers of N penetrations contained a unique class of cells with excitatory responses restricted to the two spectral ends, endspectral double-peak cells. A model is proposed for the color organization of layer 4 in foveal striate cortex, with red and blue zones in register with alternate cytochrome oxidase “blobs” of layers 2 and 3, white zones in register with interblob centers, and yellow and green zones in between.

In this paper we apply the two methods described in the companion paper (4) to experimentally recorded spike trains from two preparations, the crayfish claw and the cat striate cortex. Neurons in the crayfish claw control system produced favored patterns in 23 of 30 spike trains under a variety of experimental conditions. Favored patterns generally consisted of 3-7 spikes and were found to be in excess by both quantized and template methods. Spike trains from area 17 of the lightly anesthetized cat showed favored patterns in 16 of 27 cases (in quantized form). Some patterns were also found to be favored in template form; these were not as abundant in the cat data as in the crayfish data. Most firing of the cat neurons occurred at times near stimulation, and the observed patterns may represent stimulus information. Favored patterns generally contained up to 7 spikes. No obvious correlations between identified neurons or experimental conditions and the generation of favored patterns were apparent from these data in either preparation. This work adds to the existing evidence that pattern codes are available for use by the nervous system. The potential biological significance of pattern codes is discussed.

We have conducted physiological and psychophysical experiments to identify possible neural substrates of the perception of apparent motion. We used identical sequences of flashed stimuli in both sets of experiments to better compare the responses of cortical neurons and psychophysical observers. Physiological data were obtained from two cortical visual areas, striate cortex (V1) and the middle temporal area (MT). In the previous paper we presented evidence that neuronal thresholds for direction selectivity in extrastriate area MT were similar to psychophysical thresholds for motion perception at the largest effective interflash interval, and thus speed, for a given eccentricity. We now examine physiological and psychophysical thresholds for a broad range of speeds to determine whether such a correspondence exists for speeds below the upper threshold considered in the previous paper. Stimuli were presented in stroboscopic motion of constant apparent speed while the spatial and temporal interflash intervals were systematically varied. For each neuron we measured the largest spatial interval that elicited directionally selective responses at each of several apparent speeds. We calculated the composite performance of neurons in both MT and V1 by averaging the spatial interval necessary for direction selectivity at each apparent speed. We employed the same apparent-motion stimuli for psychophysical experiments with human subjects in which we measured the spatial interval necessary for the perception of motion over a similar range of apparent speeds. We obtained a composite profile of psychophysical performance by averaging thresholds across subjects at each apparent speed. For high apparent speeds, physiological data from MT, but not V1, corresponded closely to the psychophysical data as suggested in the preceding paper. For low apparent speeds, however, physiological data from MT and V1 were similar to each other and to the psychophysical data. It would appear, therefore, that neurons in either V1 or MT could mediate the perceptual effect at low speeds, whereas MT is a stronger candidate for this role at high speeds. We suggest that the neuronal substrate for apparent motion may be distributed over multiple cortical areas, depending upon the speed and spatial interval of the stimulus.