Eye movement-related activities in cells of the lateral suprasylvian cortex of the cat

Investigation of eye movement-related activities and photic responsiveness using behaving cats demonstrated distinctive representations of eye movement signals in different areas of the lateral suprasylvian cortex: visual reafference in the medial bank of the middle suprasylvian sulcus and non-visual signals (proprioceptive reafference or efference copy) in the lateral bank.     

Neuronal responsiveness to three-dimensional motion in cat posteromedial lateral suprasylvian cortex

The neuronal responsiveness to three-dimensional (3D) motion in cat posteromedial lateral suprasylvian (PMLS) cortex was studied using a computer-controlled, stereoscopic 3D graphic display capable of reproducing the major visual cues for natural 3D motion, including motion disparity, size, texture, and shading changes. The animals were anesthetized with nitrous oxide supplemented with alphaxalone, and paralysis prevented eye movement. Systematic investigation of neuronal responsiveness to 3D motions in 26 different directions revealed that more than half of the PMLS cells were selectively responsive to approaching (AP cells, 112 of 271) or recessive motion (RC cells, 64 of 271). The remaining cells were selectively responsive to frontoparallel motion (FP cells, 49 of 271) or nonselectively responsive to motion in multiple directions (NS cells, 46 of 271). The dependency on these visual cues was investigated as a reduction in the response amplitude or the response selectivity for the removal of a single cue from the motion stimuli containing the full visual cues. The AP and RC cells showed a strong dependency on the motion disparity cue, moderate dependency on the size cue, and weak dependency on the texture and shading cues. The FP cells showed no dependency on those visual cues. The cue dependency analysis indicated the existence of nonlinear interactions between those visual cues. Comparison of the responses to a combination of the motion disparity and size cues with the summed responses to each of the individual cues revealed that the responses to the combined cues are roughly predicted as a linear sum between the preferred responses. This comparison also showed nonlinear summation between the nonpreferred responses, i.e., responses to the combined cues were smaller than the summed responses. A similar quasilinear summation of the preferred responses between the two eyes and a nonlinear summation of the nonpreferred responses were found in the AP and RC cells for the motion disparity stimulus. All of these observations indicate that quasilinear and nonlinear interactions of the responses to various stimulus elements underlie the 3D motion responsiveness of the PMLS cells. Received: 6 January 1998 / Accepted: 23 April 1998     

Spatial and temporal properties of neurons of the lateral suprasylvian cortex of the cat

Neurons in the posteromedial lateral suprasylvian cortex (PMLS) of cats were recorded extracellularly to investigate their response to stimulation by bars and by sinusoidal gratings. Two general types of cells were identified: those that modulated in synchrony with the passage of drifting bars and gratings and those that responded with an unmodulated increase in discharge. Both types responded to contrast reversed gratings with a modulation of activity: the cells that modulated to drifting gratings modulated to the first harmonic of contrast reversed gratings (at appropriate spatial phase and frequency), whereas those that did not modulate to drifting gratings always modulated to the second harmonic of contrast reversed gratings. No cell had a clear null point. Nearly all cells were selective for spatial frequency. The preferred frequency ranged from 0.1 to 1 cycles per degree (cpd), and selectivity bandwidths (full width at half height) were around two octaves. Preferred spatial frequency was not correlated with receptive field size, but bandwidth and receptive field size were positively correlated. Preferred spatial frequency decreased with eccentricity, at about 0.05 octaves/deg. The response of all cells increased as a function of grating contrast up to a saturation level. The contrast threshold for response to a grating of optimal parameters was approximately 1% for most cells and the saturation contrast approximately 10%. The contrast gain was approximately 25 spikes/s per log unit of contrast. All cells were tuned for temporal frequency, preferring frequencies from approximately 3 to 10 Hz, with a selectivity bandwidth approximately 2 octaves. For some cells, the spatial selectivity did not depend on the temporal frequency and vice versa. Others were spatiotemporally coupled, with the preferred temporal frequency being lower at high than at low spatial frequencies, and the preferred spatial frequency lower at high than at low temporal frequencies. Previous results showing broad velocity tuning to a bar were replicated and found to be predictable from the combined spatial and temporal tuning of PMLS cells and the Fourier spectrum of a bar. Preferred temporal frequency steadily decreased with eccentricity, at 0.025 octaves/deg. The results for PMLS cells are compared with those of other visual areas. Acuity and spatial preference and selectivity bandwidth is comparable to all areas except area 17, where they are a factor of about two higher. Temporal selectivity in PMLS is as fine as observed in other areas. The possibility that PMLS cells may be involved with motion detection and detection of motion in depth is discussed.     

Global motion integration in the postero-medial part of the lateral suprasylvian cortex in the cat

In cats, the postero-medial part of lateral suprasylvian cortex (PMLS) is generally considered a key area for motion processing. While behavioral studies have indeed supported the role of PMLS cortex in higher order motion integration (Cereb Cortex 6:814–822, 1996), there is no evidence that individual PMLS cells can perform such analysis (Vis Neurosci 5:463–468, 1990; J Neurophysiol 63:1529–1543, 1990). Given the fundamental importance of understanding the neural substrate subtending higher order motion processing, we investigated whether PMLS neurons can signal the direction of motion of complex random dot kinematograms (RDKs) wherein comprising elements do not provide any local coherent motion cues. Results indicated that most PMLS cells (82%) can integrate the displacement of individual elements into a global motion percept. Their large receptive fields allowed the integration of motion for elements separated by large spatial intervals (up to 4°). In most cases, the analysis of complex RDK motion necessitated the contribution of the area of the visual field beyond the classical receptive field. None of the complex RDK-sensitive cells were found to be pattern-motion selective when tested with plaid patterns. Our results provide the first evidence that receptive fields of PMLS neurons can perform global motion analysis and support the behavioral evidence that this area is implicated in complex motion processing (Cereb Cortex 6:814–822, 1996). It also further corroborates the findings that PMLS neurons cannot signal the true direction of a plaid pattern (Vis Neurosci 5:463–468, 1990; J Neurophysiol 63:1529–1543, 1990). Providing that these same neurons can signal the direction of complex RDKs, there may be distinct cortical mechanisms for processing different types of complex motion.     

Responses of neurons in the cat posteromedial lateral suprasylvian cortex to moving texture patterns

The posteromedial lateral suprasylvian cortex represents a point of convergence between the geniculostriate and extrageniculostriate visual pathways. Given its purported role in motion analysis and the conflicting reports regarding the texture sensitivity of this area, we have investigated the response properties of cells in PMLS to moving texture patterns ("visual noise"). In contrast to previous reports, we have found that a large majority of cells (80.1%) responds to the motion of a texture pattern with sustained discharges. In general, responses to noise were more broadly tuned for direction compared to gratings; however, direction selectivity appeared more pronounced in response to noise. The majority of cells was selective for drift velocity of the noise pattern (mean optimal velocity: 26.7 degrees /s). Velocity tuning was comparable to that of its principal thalamic input, the lateral posterior pulvinar nucleus. In general, responsiveness of cells in the posteromedial lateral suprasylvian cortex increased with increasing texture element size, although some units were tuned to smaller element sizes than the largest presented. Finally, the magnitude of these noise responses was dependent on the area of the visual field stimulated. In general, a stimulus corresponding to roughly twice the size of the receptive field was required to elicit an equivalent half-maximal response to that for gratings.The results of this study indicate that the majority of cells in the posteromedial lateral suprasylvian cortex can be driven by the motion of a fine texture field, and highlight the importance of this area in motion analysis.     

Functional compensation in the lateral suprasylvian visual area following bilateral visual cortex damage in kittens

Summary Previous studies have shown that functional compensation is present in the cat's posteromedial lateral suprasylvian (PMLS) area of cortex after damage to areas 17, 18, and 19 (visual cortex) early in life but not after damage in adults. These studies all have investigated animals with a unilateral visual cortex lesion, whereas all behavioral studies of compensation for early visual cortex damage have investigated animals with a bilateral lesion. In the present experiment, we investigated whether functional compensation also is present in PMLS cortex after a bilateral visual cortex lesion early in life. We recorded from single neurons in the PMLS cortex of adult cats that had received a bilateral lesion of areas 17, 18, and 19 on the day of birth or at 8 weeks of age. We found that PMLS cells in both groups of cats had functional compensation (normal direction selectivity and ocular dominance) similar to that seen after a unilateral lesion at the same ages. These results are consistent with the hypothesis that PMLS cortex is involved in the behavioral compensation seen after early visual cortex damage. In addition, the results indicate that inputs from contralateral visual cortex are not necessary for the development of functional compensation seen in PMLS cortex.     

Visual response properties of neurons in the middle and lateral suprasylvian cortices of the behaving cat

Summary The visual response properties of cells in the middle (MS) and lateral (LS) suprasylvian cortices were studied in alert cats, which were trained to fixate a spot of light and maintain fixation when a second test light was introduced in the midst of fixation. This second light served to test for visual sensitivity, and it could be moved at different speeds in any direction under computer control. Over half of the cells exhibited a visual response. With a small spot of light, most cells were directionally selective and responded better to a moving spot than to a stationary one. In some cases movements of the spot in the non-preferred direction revealed an inhibitory process. The visual receptive fields were large and often extended into the ipsilateral hemifield, though the centers of the receptive fields were usually in the contralateral field. We used Fourier analysis to quantify directional selectivity and compared these results to other commonly used measures of directional selectivity. Compared to cells in MS, there was a higher incidence of visual cells in LS and the visual cells were more directional. We also made comparisons between our results and those found in anesthetized cats and awake monkeys.     

Neuronal responsiveness in areas 19 and 21a,and the posteromedial lateral suprasylvian cortex of the cat

Responsiveness to slits and pattern stimuli was quantified in a total of 68 cells sampled in the posterior extreme of the lateral suprasylvian (PS) cortex as response indices. The cells were studied in relationship to their locations in several subareas of the PS cortex, including areas 19 (n=15) and 21a (n=32) and the posteromedial lateral suprasylvian cortex (PMLS; n=21). These subareas were identified based on retrograde labelling from area 17 and also supplemented with photic responsiveness. This analysis revealed that each cortical area contains cells expressing different combinations of stimulus features. Area 19 contained two major groups of cells: (1) those with strong end-stop selectivity combined with moderate orientation or direction selectivity, and (2) those with weak end-stop selectivity combined with strong orientation selectivity. The groups of cells with strong or moderate orientation selectivity showed a strong preference for stripe over visual noise patterns and relatively large modulatory responses to motion of individual stripes. The PMLS contained one major group of cells with strong end-stop and direction selectivities and with poor orientation selectivity. They also showed stronger preference for visual noise than cells in the other cortical areas and rather weak modulatory responses. Area 21a contained only one group of cells with strong orientation selectivity and length summation property rather than end-stop selectivity, and they also lacked direction selectivity. These cells exhibited a strong preference for stripe patterns and moderate or weak modulatory responses. Altogether, these findings indicate that each cortical area is specialized in expressing different stimulus features. The two groups of cells in area 19 may encode the position and motion of discontinuous visual elements such as corners and line ends and continuous elements such as lines and edges. PMLS cells may encode the motion of single elements or associated motion of multiple discontinuous elements such as textures and backgrounds. Area 21a cells may specifically encode the orientation of long, continuous elements such as lines and edges. In support of this view, two types of statistical analyses demonstrated that the combinations of the response properties expressed in individual PS cells are highly correlated with their locations in cortical areas and that the anatomical locations of individual PS cells are reliably predicted from the sets of response indices expressed in these cells.     

Vestibulo-thalamic projection to the anterior suprasylvian cortex of the cat

Summary Suggestive evidence as to the site of a major thalamic relay of the vestibular projection to the anterior suprasylvian (ASS) cortex in the cat has been obtained using the retrograde axonal transport of horseradish peroxidase. The thalamo-cortical neurons are located in several patches surrounding the posterior margins of the ventro-basal complex (VB). This area also was found to receive vestibulo-thalamic projections. It comprises different nuclear groups known to carry somatic, accoustic, visual or combined information, which possibly have certain functions related to kinaesthesia and body orientation in common.Abbreviations ANS ansate sulcus - ASSS anterior suprasylvian sulcus - CM, N centrum medianum - CL, N centralis lateralis - C.r Corpus restiformis - D, N vestibularis descendens - i.c., N intercalatus - L, N vestibularis lateralis - LD, N lateralis dorsalis - LG, N geniculatus lateralis - LP, N lateralis posterior - M, N vestibularis medialis - MG, N geniculatus medialis - mcMG pars magnocellularis of MG - MD, N medialis dorsalis - N.c., N cuneatus - N. in. VIII, N interstitialis of the VIIIth cranial nerve - N. pr. V principal sensory trigeminal nucleus - N. tr. sp. V nucleus of the spinal trigeminal tract - p.h., N praepositus hypoglossi - Pu pulvinar - S, N vestibularis superior - SG, N suprageniculatus - VL, N ventralis lateralis - VPL, N ventralis posterolateralis - VPM, N ventralis posteromedialis - VI, X, XII motor cranial nerve nuclei - y, z small cell groups of Brodal and Pompeiano Supported by Deutsche Forschungsgemeinschaft, SFB 70     

The properties of convergence eye movements evoked from the rostral and caudal lateral suprasylvian cortex in the cat

Convergence eye movements were evoked in the lateral suprasylvian cortex (LS cortex) in the cat. Three effective regions were found: the rostral and caudal parts of the postero-medial LS cortex (the PMLS) and the rostral part of the postero-lateral LS cortex (the PLLS). These three areas represent the central and paracentral visual fields in the published retinotopic map (Palmer et al., 1978). Convergence eye movements evoked from the caudal PMLS were divided into two groups based on their latencies; the short-latency components (SLC) and long-latency components (LLC). The SLC and the LLC had differences in their symmetry of right and left eye movements during vergence eye movement. The SLC had symmetric right and left eye components and the LLC had dominant contralateral eye components. In the rostral PMLS, latencies of evoked convergence eye movement were comparable to those of the caudal PMLS, but they did not divided into two groups. Convergence eye movements evoked from the PLLS had longer latencies than those from the PMLS and asymmetric right and left eye components. It is suggested that different subregions in the LS cortex contribute to the control of convergence eye movement, playing different roles.     

Receptive-field characteristics of single neurons in lateral suprasylvian visual area of the cat.

The visual receptive fields of 213 cells in the lateral suprasylvian visual cortex (LS, or Clare-Bishop area) were studied in cats anesthetized with nitrous oxide. Eighty-one percent of the cells were directionally selective. They responded poorly to stationary stimuli flashed on or off, but gave a directionally selective response to stimuli moving through the receptive field. Most of these had a single preferred direction and an opposite null direction. They typically responded to a range of directions of stimulus movement from 45 to 90 degrees to either side of the preferred direction. Small stimuli (1-2 degrees or smaller) typically were effective and 87% of the directionally selective cells showed spatial summation. About 32% had inhibitory mechanisms which decreased the response of the cell if the stimulus exceeded a maximum size. There was little or no evidence that LS area cells were orientation selective or sensitive to variations in stimulus shape independent of size.     

The role of the lateral suprasylvian visual cortex of the cat in object-background interactions: Permanent deficits following lesions

The contribution of the lateral suprasylvian cortex to pattern recognition was studied by behavioural detection experiments in combination with bilateral lesions of different parts of the lateral suprasylvian areas (LSA) and area 7 in seven cats. In a two-alternatives forced choice task the cats had to discriminate simple outline patterns which were additively superimposed on a structured visual background made up of broadband Gaussian noise. For various stimulus conditions (moving or stationary patterns and/or background) the detection probability (P _D) of the cats was measured as a function of the signal to noise ratio (S/N). Each cat was tested before and after the lesion. Four different types of lesion could be distinguished depending on their extent: (1) lesion of parts of the (LSA); (2) lesion of parts of the LSA with undercutting of areas 17, 18 and 19; (3) lesion of area 7; (4) lesion of area 7 and parts of the LSA.

Simple and complex visual motion response properties in the anterior medial bank of the lateral suprasylvian cortex

The cortical regions surrounding the suprasylvian sulcus have previously been associated with motion processing. Of the six areas originally described by Palmer et al. [J Comp Neurol 177 (1978) 237], the posteromedial lateral suprasylvian (PMLS) cortex has attracted the greatest attention. Very little physiological information is available concerning other suprasylvian visual areas, and in particular, the anteromedial lateral suprasylvian cortex (AMLS). Based on its cortical and sub-cortical connectivity patterns, the AMLS cortex is a likely candidate for higher-order motion processing in cat visual cortex. We have investigated this possibility by studying the receptive field sensitivity of AMLS neurons to complex motion stimuli. Neurons in AMLS cortex exhibited large (mean of 354 degrees (2)) and complex-like receptive fields, and most of them (74%) were classified as direction selective on the basis of their responses to sinusoidal drifting gratings. Most importantly, direction selectivity was present for complex motion stimuli. A subset of the neurons sampled (eight of 38 cells; 21%) exhibited pattern-motion selectivity in response to moving plaid patterns. The capacity of AMLS neurons to signal higher-order stimuli was further supported by their selectivity to moving complex random-dot kinematograms. Finally, 45% of 20 neurons were direction selective to a radial optic flow stimulus. Overall, these results suggest that AMLS cortex is involved in higher-order analyses of visual motion. It is possible that the AMLS cortex represents a region between PMLS and the anterior ectosylvian visual area in a functional hierarchy of areas involved in motion integration.     

Phase- and position-disparity coding in the posteromedial lateral suprasylvian area of the cat

The posteromedial lateral suprasylvian area of the cat is known to be involved in the analysis of motion and motion in depth. However, it remains unclear whether binocular cells in the posteromedial lateral suprasylvian area rely upon phase or positional offsets between their receptive fields in order to code binocular disparity. The present study aims at clarifying more precisely the neural mechanisms underlying stereoperception with two objectives in mind. First, to determine whether cells in the posteromedial lateral suprasylvian area code phase disparities. Secondly, to examine whether the cells sensitive to phase disparity are the same as those which code for position disparities or whether each group represent a different sub-population of disparity-sensitive neurons. We investigated this by testing both types of disparities on single neurons in this area. The results show that the vast majority of cells (74%), in the posteromedial lateral suprasylvian area, are sensitive to relative interocular phase disparities. These cells showed mostly facilitation (95%) and a few (5%) summation interactions. Moreover, most cells (81%) were sensitive to both position and phase disparities.The results of this study show that most binocular cells in the posteromedial lateral suprasylvian area are sensitive to both positional and phase offsets which demonstrate the importance of this area in stereopsis.     

Effects of lesioning the anterior suprasylvian cortex on visuo-motor guidance performance in the cat

Summary Seven cats were trained to press a lever that moved in front of them at an adjustable speed and at random from left to right or from right to left. Efficient presses were reinforced by food. After measuring accuracy and latency of pressing the lever, the animals underwent bilateral ablation of the suprasylvian (SS) cortex; in three animals the lesions involved its anterior aspect; in two animals, they were restricted to its middle portion; two others cats had lesions of both anterior and the middle SS cortex. No long-lasting postoperative deficits were observed in any group when the lever remained immobile. On the other hand, the scores after anterior SS lesions were severely deteriorated, when presses had to be performed on the moving lever. No such deficits were noticed when the ablations were restricted to the middle SS. These results suggest that the cat anterior suprasylvian cortex (that includes parts of areas 5 and 7) plays a determinant role in the spatial adjustment of a visually guided (or visually triggered) forelimb movement.This work was supported by the following grants: ERA - CNRS 411; ATP 36-22; Fondation pour la Recherche Medicale Française     

Cat lateral suprasylvian cortex: Y-cell inputs and corticotectal projection

Retinal Y-cells activate most cells in the deep layers of the cat's superior colliculus via an indirect pathway involving the occipital cortex. The lateral suprasylvian area seems to be an important source of visual input to the deep collicular strata but it is unclear whether Y-cell influences reach this extrastriate area and, hence, whether this area participates in the indirect Y-cell pathway. In this study, retinal influences on the posteromedial lateral suprasylvian area (PMLS) were studied in anesthetized cats. Responses to electrical stimulation of the optic disk (OD) and optic chiasm (OX) were recorded in single units in PMLS and in neurons of the dorsal lateral geniculate nucleus (LGNd) that were antidromically driven from PMLS. Virtually all PMLS cells (99%; 99/100) exhibited small differences (less than or equal to 0.8 ms) between OD- and OX-activation latency, indicating that they were driven by a pathway originating in rapidly conducting Y-cell axons. A small number of PMLS cells (17%; 20/118) had very short activation latencies (less than or equal to 3.2 ms from OX), comparable to those of cells in areas 17 and 18 receiving monosynaptic inputs from geniculate Y-cells. Further, LGNd cells with latency behaviors typical of Y-cells could be antidromically driven from PMLS, confirming that geniculate Y-cells project directly to PMLS. Most PMLS cells (83%; 98/118), though exhibiting small OD-OX latency differences, had absolute latencies too long to be attributed to direct inputs from geniculate Y-cells (3.3-8.5 ms from OX). Thus Y-cells in the LGNd influence most PMLS cells by way of a multisynaptic pathway. PMLS cells antidromically activated from the superior colliculus were driven only by this multisynaptic Y-cell input. Total conduction time from the retina through PMLS to the colliculus corresponds closely to the latency of the indirect Y-cell activation observed in the deep collicular layers. These results support the view that the lateral suprasylvian cortex constitutes an important source of visual input to the cat's deep collicular layers and, more generally, that the extrastriate visual cortex may figure prominently in the cortical control of gaze.     

Contralateral corticofugal projections from the lateral,suprasylvian and ectosylvian gyri in the cat

Summary Contralateral corticofugal projections were investigated following multiple injections of a mixture of tritiated leucine and proline into the lateral, postlateral, suprasylvian and ectosylvian gyri of adult cats. Transported label was found in several Contralateral subcortical regions. These included the claustrum, caudate-putamen, thalamic intralaminar nuclei, pretectum, and the superior and inferior colliculi. These results show that the crossed corticofugal projections are common in the cat and are more extensive than has been previously reported.Abbreviations AC Anterior Commissure - AM Anteromedial Nucleus - AV Anteroventral Nucleus - Cd Caudate - CeM Central Medial Nucleus - CL Central Lateral Nucleus - Cl Claustrum - CM Centromedian Nucleus - GP Globus Pallidus - IC Inferior Colliculus - LD Laterodorsal Nucleus - LGd Dorsal Nucleus of the Lateral Geniculate complex - LP Lateral Posterior Nucleus - MD Mediodorsal Nucleus - MG Principal Nucleus of the Medial Geniculate complex - OT Optic Tract - Pa Anterior Pretectal Nucleus - Pl Pulvinar Nucleus - Put Putamen - Re Reuniens Nucleus - RN Red Nucleus - SC Superior Colliculus - SN Substantia Nigra - TRC Tegmental Reticular Nucleus, central division - VA Ventral Anterior Nucleus of thalamus - VB Ventrobasal Complex of thalamus - 3 Oculomotor Nucleus     

Differences of visual field representation in the medial and lateral banks of the suprasylvian cortex (PMLS/PLLS) of the cat

Summary We have studied the orderliness of representation of visual space in the medial and lateral banks of the middle suprasylvian sulcus. Penetrations were made either parallel to the sulcus, in one bank or the other, or vertical, thus crossing the sulcus between the postero-medial (PMLS) and posterolateral (PLLS) divisions of this area. In some cases we found clear evidence for topographical order in the representation of the visual field with a tendency (greater in PMLS than in PLLS) for the receptive fields of cells recorded deeper in the walls of the sulcus to lie closer to the area centralis, but along many penetrations the receptive fields were so large and so scattered that no retinotopic arrangement could be discerned. In PMLS the receptive fields of the majority of units we studied were centred below and close to the horizontal meridian, whereas in PLLS they were distributed over both the upper and lower visual fields with an over-representation of the upper field. Receptive fields were significantly larger in PLLS (mean field area = 442.2 deg²) than in PMLS (mean area = 154.4 deg²); there was also less clear correlation between receptive field size and eccentricity in PLLS (correlation coefficient = +0.25) than in PMLS (corr. coeff. = +0.72). Analysis of the distance between the receptive field centres of consecutively recorded units demonstrated that the mean scatter in both PMLS and PLLS amounts to about half the average receptive field diameter. In summary the topographical representation of visual space is less orderly in PLLS, and may involve a wider area of the visual field. These findings may relate to the segregated visual cortical and extrageniculate thalamic connections that the medial and lateral banks of the LS receive.