Topographic organization of orientation columns in the cat visual cortex

Summary Three-dimensional reconstructions of the orientation column system were obtained from the visual cortex of four cats using the deoxyglucose technique. One cat had normal visual experience, one was monocularly deprived and two had selective experience with vertical and horizontal contours, respectively. In areas 17 and 18 orientation columns form a remarkably regular system of equally spaced parallel bands whose trajectory is orthogonal to the borderline between areas 17 and 18. This topographic organization is resistant to manipulations of early visual experience.     

Bilateral projections from the visual cortex to the striatum in the cat

Summary Direct projections from visual areas 17, 18, 19, and lateral suprasylvian visual area (LS) to the striatum were searched for in 12 adult cats using the autoradiographic technique to detect neuronal pathways. Striatal labels were found only after injections in areas 19 and LS. Projections homolateral to the injection sites were observed from both areas to the head and body of the caudate nucleus and to the putamen. Contralateral projections were found from both areas 19 and LS: however, area 19 did not project to the contralateral putamen. The extent of contralateral projections was smaller and they were confined within the same regions as the homolateral ones. Silver grains were often arranged in cluster-like patches, which were more evident ipsilaterally, in the head of the caudate nucleus and after injections in area LS.The present data support the view of a not strictly topographical segregation of striatal projections from the cat visual cortex.Supported by a grant from the CNR, Rome, Italy     

Identification of the projection from the visual cortex to the claustrum by anterograde axonal transport in the cat

Summary Visual cortex, including areas 17, 18, and sometimes 19, was injected with tritiated leucine. Terminal labelling could be detected by autoradiography in the dorsocaudal part of the ipsilateral claustrum in all cases.     

Response covariance in cat visual cortex

Summary The activity of pairs of neurons in the visual cortex (area 17) of anaesthetized, paralysed cats was recorded using two independently manipulated micropipettes. The number of spikes in the evoked responses of pairs of single neurons were analyzed for response covariance. Responses of the majority of cell pairs (83%) did not covary. Covariance was restricted to closeby neurons with distances of less than 150 m and with identical orientation and ocular dominance preference.This work was partially supported by grants NS10332 and EY03796     

Retinotopic order is surprisingly good within cell columns in the cat's lateral suprasylvian cortex

Summary The retinotopic map in the striate-recipient region of the cat's lateral suprasylvian cortex (referred to here as the lateral suprasylvian area (LS)) has generally been described as quite disorderly. The disorder is commonly attributed to receptive field scatter within cell columns, reflecting the very large size of receptive fields. However, scatter within columns has never been investigated. In the experiments reported here, we examined the receptive field scatter of cells in columns, and also the scatter of a limited sample of their afferents arising from areas 17 and 18. To measure post-synaptic receptive field scatter, electrode penetrations were made parallel to columns in LS, with the electrode approaching from the medial side, traversing the suprasylvian gyrus and emerging into the suprasylvian sulcus. In all 13 such penetrations, receptive fields were clustered together despite their large size. Their centers were scattered over a region that occupied on average less than 20% of the largest field in the column. In contrast, in columns in areas 17 and 18 receptive field centers reportedly are dispersed over regions about equal to the largest of the fields (Hubel and Wiesel 1962, 1965, 1974).The scatter of afferents' receptive fields was assessed anatomically by measuring the overlap between patches of different anterograde tracers in LS. These patches represented terminal labeling from two adjacent or overlapping tracer injections in area 17. While a large degree of overlap would be predicted if afferents have substantial scatter, we found the overlap to be small unless the two injection sites themselves were highly overlapping.Scatter in afferents' receptive fields was measured more directly by physiological recording. In previous experiments, cells in LS were silenced by the local injection of kainic acid, and responses were recorded from axon terminals arising from areas 17 and 18 (Sherk 1989). We examined the receptive field scatter in three penetrations made approximately normal to the cortical surface. Scatter was modest, much less than predicted by the size of post-synaptic receptive fields. Because the degree of receptive field scatter for postsynaptic cells in LS was similar to that of inputs from areas 17 and 18, the scatter of these inputs might be entirely responsible for that seen postsynaptically. Postsynaptic receptive field scatter, on the other hand, was too small to explain the reported disorder in the map in LS.     

A study of binocular convergence in cat visual cortex neurons

Summary The average latency of cortical neuronal responses to electrical optic nerve (ON) stimulation was 3.0±0.7 s.d. msec. No significant difference between latencies to ipsi- and contralateral ON stimulation was found. Binocularly excitable cells showed almost equal response latencies to stimulation of both nerves. The average latency of subcortically recorded geniculo-cortical fibers was 0.3 msec less, but showed the same variance as that of cortical cells, suggesting that in all cases direct monosynaptic excitation of cortical cells by fibers of either ocularity is possible. Classes of ocular dominance based on electrical stimulation were positively, but not 100% correlated with classes of ocular dominance to visual stimulation. An anatomical study revealed that in cat terminals of geniculo-cortical projection are segregated to a lesser degree into ocularity stripes than in monkey. Direct monosynaptic excitation of cells by fibers of either ocularity which was found physiologically would also on these grounds appear possible for all cells.A preliminary report has been presented at the 46th German Physiological Society Meeting in Spring 1976, Pflügers Archiv, Vol. 362, Abstract No. 155, 1976     

Developmental changes of calcium currents in the visual cortex of the cat

Summary During a critical period of postnatal development the visual cortex of kittens is susceptible to experience-dependent modifications of neuronal response properties. Evidence is accumulating that these modifications are triggered by a transient neuronal calcium (Ca) influx. To further investigate this issue we measured extracellular Ca concentrations with ion-sensitive microelectrodes and compared the magnitude and the distribution of stimulus-evoked Ca fluxes in slices of the visual cortex of 4- to 5-week-old kittens and of 6-month-old adult cats. Stimulation of the white matter at 15 Hz for 8 s caused transient decreases of the extracellular Ca concentration ( Ca⁰) in slices of both age groups and in all cortical layers. However, there were developmental changes in the laminar distribution of the Ca⁰: in kittens, they were maximal in layer IV whereas in adult cats they were most pronounced in the supragranular layers. The ratios between the amplitudes of Ca⁰ in layer IV and the supragranular layers were 1.65 ± 0.26 in kittens and 0.43 ± 0.2 in adult cats. These changes in laminar distribution resemble the laminar specific decay of neuronal malleability and parallel the developmental redistribution of 1,4-Dihydropyridine-sensitive Ca channels. Because of these correlations we interpret our findings as support for the hypothesis that experience-dependent modifications are triggered by Ca influx.     

Evidence for a nicotinic component to the actions of acetylcholine in cat visual cortex

Summary Radioligand binding assays, receptor autoradiography and iontophoresis have been used to look for evidence of a nicotinic component to the actions of acetylcholine in cat visual cortex. [³H]Nicotine bound to a uniform population of high affinity binding sites in cat primary visual cortex. This binding was inhibited by nicotine agonists and antagonists but not muscarinic antagonists. The concentration of nicotinic binding sites was about 10% of that of muscarinic binding sites measured with [³H]N-methylscopolamine. The muscarinic sites were resolved into M1 and M2 subtypes. Quantitative receptor autoradiography showed that there were muscarinic sites in all layers, although they were least abundant in layer IV of area 17. In contrast, the nicotinic sites were most concentrated in layer IV in area 17. The concentration of this labelling was reduced at the 17/18 border and also at the 18/19 border. Layer I of the cingulate and suprasylvian gyri were also labelled. Electrolytic lesions of the lateral geniculate nucleus (LGN) led to a loss of nicotinic binding sites in layer IV of area 17, indicating that these sites are most likely located on the LGN terminals. Iontophoresis of mecamylamine, a nicotinic antagonist, decreased evoked responses in visual cortex, providing evidence that the [³H]nicotine binding sites are functional receptors and suggesting that the release of acetylcholine onto these receptors on the LGN terminals facilitates the input of visual information into visual cortex.     

Velocity sensitivity mechanisms in cat visual cortex

Summary To understand why some cells in the visual cortex respond to high stimulus velocities while others fail to do so, a sample of 71 of such cells were examined for their responses to stationary presented stimuli as well as to moving edges or slits of different widths. When presented with stationary stimuli it was found that cells which respond best to slowly moving stimuli generally have tonic discharges, long time to peak latencies and often long minimal durations of stimulation. In contrast, cells which respond preferentially to fast stimuli have phasic discharges, short latencies and short critical durations of stimulation when presented with stationary flashed slits. In the latter type of cells the responses to very fast stimulus movement were abolished selectively when contrast and width of the stimulus were not optimal. A few cells exhitited a velocity-response (VR) curve with a central dip indicating good responsiveness to either slow or fast movement but little to medium velocities. These cells responded both phasically and tonically to stationary slits and the latency of the tonic and phasic responses corresponded well to the latency of the responses at low and high velocities, respectively. It is suggested that the ability of phasic cells to respond to high velocities is linked to their limited need for temporal summation.Supported by an NFWO grant     

The pattern of ocular dominance columns in flat-mounts of the cat visual cortex

Summary Ocular dominance (OD) columns in the cat visual cortex were visualized with autoradiography after intravitreal injection of (³H)proline. Extending previous studies, a flat-mount technique was applied that enabled the analysis of the distribution of label throughout extensive regions of the visual cortex without requiring reconstructions from serial sections. OD-columns were confined to layer IV and consisted of isolated patches and short bands. The latter were parallel to each other and regularly spaced, the main trajectory being orthogonal to the 17/18 border. This pattern of the geniculo-cortical terminals was similar in the hemispheres ipsi- and contralateral to the injected eye. The mean periodicities of the OD-bands were virtually identical in the two hemispheres of the same animal: 850 m and 830 m in cat D1 and 770 m and 800 m in cat D2. However, the ipsilateral OD-columns appeared smaller, more heavily labeled and more sharply delineated than the contralateral columns.     

Direct projections from thalamic intralaminar nuclei to extra-striate visual cortex in the cat traced with Horseradish peroxidase

Summary Thalamic projections to the visual cortex were investigated using the Horseradish peroxidase tracing technique. Besides confirmation of a distinct origin of thalamic projections to striate and extra-striate visual cortex, afferents of the intralaminar nuclei (ILN) to visual cortex were demonstrated. These projections of ILN were shown to be specific in that they terminate in areas 18, 19 and Clare Bishop but not area 17. The coupling of these intralaminar projections on to the extra-striate visual system is considered with respect to orientation of gaze.     

Differential responsiveness of simple and complex cells in cat striate cortex to visual texture

Summary The responsiveness of 254 simple and complex striate cortical cells to various forms of static and dynamic textured visual stimuli was studied in cats, lightly anaesthetised with N₂O/O₂ mixtures supplemented with pentobarbitone.Simple cells were unresponsive to all forms of visual noise presented alone, although about 70% showed a change in responsiveness to conventional bar stimuli when these were presented on moving, rather than stationary, static-noise backgrounds. Bar responses were depressed by background texture motion in a majority of cells (54%), but were actually enhanced in a few instances (16%).In contrast, all complex cells were to some extent responsive to bars of static visual noise moving over stationary backgrounds of similar texture, or to motion of a whole field of static noise. The optimal velocity for noise was generally lower than for bar stimuli.Since moving noise backgrounds were excitatory for complex cells, they tended to reduce specific responses to bar stimulation; in addition, directional bias could be modified by direction and velocity of background motion.Complex cells fell into two overlapping groups as regards their relative sensitivity to light or dark bars and visual noise. Extreme examples were insensitive to conventional bar or edge stimuli while responding briskly to moving noise.In many complex cells, the preferred directions for motion of noise and of an optimally oriented black/white bar were dissimilar.The ocular dominance and the degree of binocular facilitation of some complex cells differed for bar stimuli and visual texture.Preliminary evidence suggests that the deep-layer complex cells (those tolerant of misalignment of line elements; Hammond and MacKay, 1976) were most sensitive to visual noise. Superficial-layer complex cells (those preferring alignment) were less responsive to noise.Only complex-type hypercomplex cells showed any response to visual noise.We conclude that, since simple cells are unresponsive to noise, they cannot provide the sole input to complex cells. The differences in the response of some complex cells to rectilinear and textured stimuli throw a new light on their rôle in cortical information-processing. In particular, it tells against the hypothesis that they act as a second stage in the abstraction of edge-orientation.     

Restriction of visual experience to a single orientation affects the organization of orientation columns in cat visual cortex

Summary and Conclusions In six dark reared, 4-weak-old kittens visual experience was restricted to contours of a single orientation, horizontal or vertical, using cylindrical lenses. Subsequently, the deoxyglucose method was used to determine whether these artificial raising conditions had affected the development of orientation columns in the visual cortex. After application of the deoxyglucose pulse one hemifield was stimulated with vertical, the other with horizontal contours. Thus, from interhemispheric comparison, changes in columnar systems corresponding to experienced and inexperienced orientations could be determined. The following results were obtained: (1) Irrespective of the restrictions in visual experience, orientation columns develop in areas 17, 18, 19 and in the visual areas of the posterior suprasylvian sulcus. (2) Within area 17, spacing between columns encoding the same orientations is remarkably regular (1 mm), is not influenced by selective experience and shows only slight interindividual variation. (3) In non-striate areas the spacing of columns is less regular and the spatial frequency of the periodicity is lower. (4) The modifiability of this columnar pattern by selective experience is small within the granular layer of striate cortex but substantial in non-granular layers: Within layer IV columns whose preference corresponds to the experienced orientation are wider and more active than those encoding the orthogonal orientation but the columnar grid remains basically unaltered. Outside layer IV the columnar system is maintained only for columns encoding the experienced orientations. The deprived columns by contrast frequently fail to extend into non-granular layers and remain confined to the vicinity of layer IV. (5) These modifications in the columnar arrangement are more pronounced in striate cortex than in non-striate visual areas and, within the former, more conspicuous in the central than in the peripheral representation of the visual field. It is concluded that within layer IV the blue print for the system of orientation columns is determined by genetic instructions: first order cells in layer IV develop orientation selectivity irrespective of experience whereby the preference for a particular orientation is predetermined by the position in the columnar grid. Dependent on experience is, however, the expansion of the columnar system from layer IV into non-granular layers. It is argued that all distortions following selective rearing can be accounted for by competitive interactions between intracortical pathways, the mechanisms being identical to those established for competitive processes in the domain of ocular dominance columns. It is proposed that such experience dependent modifiability of connections between first and second order cells is a necessary prerequisite for the development of orientation selectivity in cells with large and complex receptive fields.This work has partially been supported by a grant from the Deutsche Forschungsgemeinschaft, SFB 50, A14Dedicated to Prof. D. Ploog on the occasion of his 60th anniversaryResearch Fellow of the Alexander-von Humboldt-Stiftung     

Two modes of cerebellar input to the parietal cortex in the cat

Summary The characteristics of cerebellar input to the parietal cortex through the ventroanterior-ventrolateral (VA-VL) complex of the thalamus were investigated in the adult cat by using combined electrophysiological and anatomical methods. Two distinct parietal regions were activated by stimulation of the cerebellar nuclei (CN). In the first region located in the depth of the bank of the ansate sulcus, stimulation of the CN induced early surface positive-deep negative potentials and late surface negative-deep positive potentials. In this cortical area, potentials of similar shape and time course were evoked at a shorter latency by stimulation of the ventrolateral part of the VA-VL complex where large negative field potentials were evoked by stimulation of the CN. After injection of the anterograde tracer Phaseolus vulgaris leucoagglutinin (PHA-L) in this part of the VA-VL complex, axon terminals of thalamocortical (TC) fibers were found in layers I, III and IV in the depth of the bank of the ansate sulcus and layers I and III in the motor cortex. In the second region located in the suprasylvian gyrus, late surface negative-deep positive potentials were evoked by stimulation of the CN and similar potentials were evoked at a shorter latency from the dorsomedial part of the VA-VL complex where large cerebellar-evoked potentials could be recorded. PHA-L injection in this thalamic region stained TC fibers and their terminals in layer I of the suprasylvian gyrus, and in layers I and III of the motor cortex. The laminar distribution of TC axon terminals in two different regions of the parietal cortex could account for the depth profiles of the cerebellar- and the thalamic-evoked potentials in each region. These results show that cerebellar information is conveyed to two separate areas in the parietal cortex by two different TC pathways.     

The distribution of degenerating axons after small lesions in the intact and isolated visual cortex of the cat

Summary The extent of the spread of axonal degeneration was investigated in the visual cortex of the cat after making small lesions restricted to the grey matter. Two series of experiments were undertaken. In the first, normal adult cats were used, and in the second, the cortex of the postlateral gyrus was isolated from its extrinsic afferents by surgical undercutting 3 months before making the lesions. The results were similar in the two series in most respects. 1. Horizontal fibres extended in considerable numbers for some 500 m from the lesion, mainly in layers I, III/IV and V, a few reaching 2–3 mm. These fibres were better seen in the intact than in the isolated cortex. Their spread was usually asymmetrical, being greater posteromedially than anterolaterally. 2. Oblique axons ran downwards from the middle layers into layers V and VI, or upwards into layers I and II. 3. Axons arising from layers II to VI descended vertically into the white matter. Degeneration patterns after lesions in areas 17 and 18 were compared.     

Single neuron activity related to natural vestibular stimulation in the cat's visual cortex

Summary This study examines the possibility of a vestibular input to the visual cortex using chronically implanted cats subjected to horizontal sinusoïdal rotation in the dark. In areas 17 and 18 the activity of respectively 14% and 11% of units was modified by vestibular stimulation. Both non-specific and specific influences were observed. Specific influences (42% in area 17 and 33% in area 18) were similar to the types of responses recorded in the vestibular nuclei, and were encountered more frequently within the cortex subserving the peripheral visual field. Our results could provide a neurophysiological basis for some psychophysiological observations concerning visuo-vestibular interactions.Supported by I.N.S.E.R.M. (C.R.L. 79-53336)     

Preferred direction of movement as an element in the organization of cat visual cortex

Summary Neurones recorded close together in the cat's striate cortex prefer not only the same orientation of elongated visual stimulus but also the same direction of stimulus movement. The degree of similarity in both preferred orientation and preferred direction is greater in electrode penetrations made perpendicular to the cortical surface than in oblique penetrations. This suggests that preferred direction is organized in columnar fashion, just as is orientation.Supported by the Medical Research CouncilSupported by the Wellcome TrustSupported by the MRC     

Anatomical evidence for the projections from the basal nucleus of the amygdala to the primary visual cortex in the cat

The amygdaloid complex receives information from all sensory systems, especially from vision. In the primate, the amygdala is reciprocally interconnected with some regions of high-order visual cortices such as TE and TEO and only projects to the primary visual cortex (V1, area 17) without direct projection from V1. However, in the cat little is known about the projection from the amygdala to the primary visual cortex. In this study, anatomical study is carried out in cats to determine whether the amygdala sends feedback projection to area 17. FlouroGold, a fluorescent dye was microinjected into area 17 in cats. In the basal nucleus in the amygdala, the retrograde labeled cells (about 30% of total number of the region of interest observed) are distributed widely in an irregular manner, neither in lamina nor in group. The results provide the first anatomical evidence of the amygdale projection to area 17 in the cat, which is a widely used animal model for vision research.     

The variability of discharge of simple cells in the cat striate cortex

Summary The relationship between the variance and mean rate of discharges of simple cells in the cat striate cortex has been examined when mean rate was varied by changing either stimulus spatial frequency or contrast. In both cases, the variance was related to the mean discharge rate by an exponent of about 1.15; the relation was thus roughly linear. The discharge variance was on average 1.7 times the mean rate for data obtained from measurements of the neurones' spatial frequency tuning curves, and 1.48 times the mean for data from the response-contrast determination. However, this difference was not statistically significant.This work was partially supported by an MRC project grant to D.J. Tolhurst and by the Wellcome TrustRecipient of an MRC Research Scholarship