Torsten N. Wiesel

Receptive fields, binocular interaction and functional architecture in the cat's visual cortex

What chiefly distinguishes cerebral cortex from other parts of the central nervous system is the great diversity of its cell types and inter-connexions. It would be astonishing if such a structure did not profoundly modify the response patterns of fibres coming into it. In the cats visual cortex, the receptive field arrangements of single cells suggest that there is indeed a degree of complexity far exceeding anything yet seen at lower levels in the visual system. In a previous paper we described receptive fields of single cortical cells, observing responses to spots of light shone on one or both retinas (Hubel & Wiesel, 1959). In the present work this method is used to examine receptive fields of a more complex type (Part I) and to make additional observations on binocular interaction (Part II). This approach is necessary in order to understand the behaviour of individual cells, but it fails to deal with the problem of the relationship of one cell to its neighbours. In the past, the technique of recording evoked slow waves has been used with great success in studies of functional anatomy. It was employed by Talbot & Marshall (1941) and by Thompson, Woolsey & Talbot (1950) for mapping out the visual cortex in the rabbit, cat, and monkey. Daniel & Whitteiidge (1959) have recently extended this work in the primate. Most of our present knowledge of retinotopic projections, binocular overlap, and the second visual area is based on these investigations. Yet the method of evoked potentials is valuable mainly for detecting behaviour common to large populations of neighbouring cells; it cannot differentiate functionally between areas of cortex smaller than about 1 mm2. To overcome this difficulty a method has in recent years been developed for studying cells separately or in small groups during long micro-electrode penetrations through nervous tissue. Responses are correlated with cell location by reconstructing the electrode tracks from histological material. These techniques have been applied to CAT VISUAL CORTEX 107 the somatic sensory cortex of the cat and monkey in a remarkable series of studies by Mountcastle (1957) and Powell & Mountcastle (1959). Their results show that the approach is a powerful one, capable of revealing systems of organization not hinted at by the known morphology. In Part III of the present paper we use this method in studying the functional architecture of the visual cortex. It helped us attempt to explain on anatomical …

Receptive fields and functional architecture of monkey striate cortex

1. The striate cortex was studied in lightly anaesthetized macaque and spider monkeys by recording extracellularly from single units and stimulating the retinas with spots or patterns of light. Most cells can be categorized as simple, complex, or hypercomplex, with response properties very similar to those previously described in the cat. On the average, however, receptive fields are smaller, and there is a greater sensitivity to changes in stimulus orientation. A small proportion of the cells are colour coded.

Ferrier Lecture: Functional Architecture of Macaque Monkey Visual Cortex

Of the many possible functions of the macaque monkey primary visual cortex (striate cortex, area 17) two are now fairly well understood. First, the incoming information from the lateral geniculate bodies is rearranged so that most cells in the striate cortex respond to specifically oriented line segments, and, second, information originating from the two eyes converges upon single cells. The rearrangement and convergence do not take place immediately, however: in layer IVc, where the bulk of the afferents terminate, virtually all cells have fields with circular symmetry and are strictly monocular, driven from the left eye or from the right, but not both; at subsequent stages, in layers above and below IVc, most cells show orientation specificity, and about half are binocular. In a binocular cell the receptive fields in the two eyes are on corresponding regions in the two retinas and are identical in structure, but one eye is usually more effective than the other in influencing the cell; all shades of ocular dominance are seen. These two functions are strongly reflected in the architecture of the cortex, in that cells with common physiological properties are grouped together in vertically organized systems of columns. In an ocular dominance column all cells respond preferentially to the same eye. By four independent anatomical methods it has been shown that these columns have the form of vertically disposed alternating left-eye and right-eye slabs, which in horizontal section form alternating stripes about 400 μm thick, with occasional bifurcations and blind endings. Cells of like orientation specificity are known from physiological recordings to be similarly grouped in much narrower vertical sheeet-like aggregations, stacked in orderly sequences so that on traversing the cortex tangentially one normally encounters a succession of small shifts in orientation, clockwise or counterclockwise; a 1 mm traverse is usually accompanied by one or several full rotations through 180°, broken at times by reversals in direction of rotation and occasionally by large abrupt shifts. A full complement of columns, of either type, left-plus-right eye or a complete 180° sequence, is termed a hypercolumn. Columns (and hence hypercolumns) have roughly the same width throughout the binocular part of the cortex. The two independent systems of hypercolumns are engrafted upon the well known topographic representation of the visual field. The receptive fields mapped in a vertical penetration through cortex show a scatter in position roughly equal to the average size of the fields themselves, and the area thus covered, the aggregate receptive field, increases with distance from the fovea. A parallel increase is seen in reciprocal magnification (the number of degrees of visual field corresponding to 1 mm of cortex). Over most or all of the striate cortex a movement of 1-2 mm, traversing several hypercolumns, is accompanied by a movement through the visual field about equal in size to the local aggregate receptive field. Thus any 1-2 mm block of cortex contains roughly the machinery needed to subserve an aggregate receptive field. In the cortex the fall-off in detail with which the visual field is analysed, as one moves out from the foveal area, is accompanied not by a reduction in thickness of layers, as is found in the retina, but by a reduction in the area of cortex (and hence the number of columnar units) devoted to a given amount of visual field: unlike the retina, the striate cortex is virtually uniform morphologically but varies in magnification. In most respects the above description fits the newborn monkey just as well as the adult, suggesting that area 17 is largely genetically programmed. The ocular dominance columns, however, are not fully developed at birth, since the geniculate terminals belonging to one eye occupy layer IVc throughout its length, segregating out into separate columns only after about the first 6 weeks, whether or not the animal has visual experience. If one eye is sutured closed during this early period the columns belonging to that eye become shrunken and their companions correspondingly expanded. This would seem to be at least in part the result of interference with normal maturation, though sprouting and retraction of axon terminals are not excluded.

Functional architecture of cortex revealed by optical imaging of intrinsic signals.

Optical imaging of cortical activity offers several advantages over conventional electrophysiological and anatomical techniques. One can map a relatively large region, obtain successive maps to different stimuli in the same cortical area and follow variations in response over time. In the intact mammalian brain this imaging has been accomplished with the aid of voltage sensitive dyes1–5. However, it has been known for many years that some intrinsic changes in the optical properties of the tissue are dependent on electrical or metabolic activity6–13. Here we show that these changes can be used to study the functional architecture of cortex. Optical maps of whisker barrels in the rat and the orientation columns in the cat visual cortex, obtained by reflection measurements of the intrinsic signal, were confirmed with voltage sensitive dyes or by electrophysiological recordings. In addition, we describe an intrinsic signal originating from small arteries which can be used to investigate the communication between local neuronal activity and the microvasculature. One advantage of the method is that it is non-invasive and does not require dyes, a clear benefit for clinical applications.

Morphology and intracortical projections of functionally characterised neurones in the cat visual cortex.

The neuronal structure and connectivity underlying receptive field organisation of cells in the cat visual cortex have been investigated. Intracellular recordings were made using a micropipette filled with a histochemical marker, which was injected into the cells after their receptive fields had been characterised. This allowed visualisation of the dendritic and axonal arborisations of functionally identified neurones

Myopia and eye enlargement after neonatal lid fusion in monkeys.

THE aetiology of myopia has been studied mainly by investigating the distribution of refractive errors in human populations1. No clear conclusion has emerged, however, so the prevailing clinical attitude is that myopia can neither be prevented nor cured, but only corrected with appropriate lenses. The mechanism of myopia can be rationally analysed only if a suitable animal model is found for this refractive condition. In the literature, there are only two examples of experimental myopia. Levinsohn2 claimed that a high degree of myopia develops in young monkeys when the body is kept elevated above the head for long periods of time; his results, however, have been questioned3,4. Young5 induced myopia by exposing monkeys to a restricted visual space, but the refractive error thus obtained was relatively small. During investigations on monocular visual deprivation in monkeys6 it was noted that the eye in which the lids had been closed by suture at birth developed a high degree of myopia. We report here a study of the effects of neonatal lid fusion on the refractive state and anatomy of the macaque monkey eye.

Autoradiographic demonstration of ocular-dominance columns in the monkey striate cortex by means of transneuronal transport.

In the past few years the technique of mapping pathways in the central nervous system by anterograde axoplasmic transport of radioactive molecules has come into wide use and is now an important supplement to Nauta degeneration methods e,6,1°,13. Several investigatorsa,3,v,9,12 have noted radioactive substances in the postsynaptic ceils, which suggests that these cells take up labeled material released from the terminals 1,3,7. Grafstein 4 was the first to explore the possibility of tracing a pathway beyond the terminals of the initially labeled cells, by examining also the projections of the recipient postsynaptic neurons. By radiochemical measurements and by autoradiography, it was shown that after injection of [3H]proline and [aH]fucose into one eye of a mouse the contralateral striate cortex was more heavily labeled than the ipsilateral, and that the label was concentrated in layer IV 5,14. In the macaque monkey the geniculostriate pathway terminates in a very dense, highly localized manner, mainly in layer IV C. Furthermore, projections from the 2 eyes end in a characteristic alternating stripe-like pattern of oculardominance columns s. It occurred to us that if radioactive substances were transported transneuronally, injection of labeled material into one eye followed by autoradiography of the cortex might reveal the entire system of ocular-dominance columns. For the autoradiographic study of transneuronal transport in the primate visual system, 50/~1 of a saline solution containing L-[6-3H]fucose (2.5 mCi/ml, 13.4Ci/ mmole) and L-[3H]proline (7.5 mCi/ml, generally labeled, 6.8 Ci/mmole) was injected into the vitreous of the left eye ofa 3 kg normal Rhesus macaque. This injection was repeated 5 times at 12 h intervals (total dose 3.0 mCi). The animal was perfused with 10 ~ formalin 3 weeks after the initial injection. The lateral geniculate nucleus was cut into 20 #m frozen sections, and the striate cortex was embedded in paraffin and cut into 15/~m sections. The sections were coated with Ilford K5 emulsion, left in the dark for 2-4 months and developed in Dektol. Sections were counter-stained with thionin. In the lateral geniculate nucleus all layers receiving projections from the injected eye were strongly labeled (Fig. l A and B). The other layers showed grain counts higher than background, perhaps partly because of fibers of passage from the retina,

An animal model of myopia.

Abstract Myopia develops in macaque monkeys when their lids are surgically fused at birth and kept closed for one year. This experimental refractive error has many features in common with human myo...

The distribution of afferents representing the right and left eyes in the cat's visual cortex

Abstract The presumed anatomical basis for ocular dominance columns in the cats visual cortex was demonstrated autoradiographically. Transneuronal transport of radioactive materials following an intraocular injection of tritiated proline and fucose was used to identify the set of thalamocortical afferents representing the injected eye. In normal cats, ipsilateral to the injected eye discrete patches of silver grains were visible in layer IV and the base of layer III of areas 17 and 18. The distribution of grains in the contralateral hemisphere of area 17 was almost continuous in layer IV, but there were clear indications of periodic fluctuations in concentration. This pattern of labeling presumably reveals the overall pattern of the physiologically defined ocular dominance columns. As expected, there was a strip of heavy labeling within the monocular segment of the contralateral hemisphere and a corresponding absence of label in this region ipsilateral to the injected eye. When large portions of the fourth layer in areas 17 and 18 of the ipsilateral hemisphere were reconstructed from serial parasagittal into a system of irregular bands roughly 0.5 mm wide separated by gaps of similar width containing less label. The bands ran mediolaterally and perpendicular to the anatomical 17–18 border. The combined size of a left and right eye band was about 1 mm, both in cortex representing central and peripheral visual fields. The bands almost doubled in width within area 18. In the contralateral hemisphere the bands were less distinct due to the widespread presence of label in layer IV. This arrangement suggested that geniculocortical afferents from the two eyes share a good deal of fourth layer territory. One cat with artificially produced squint and one short-term monocularly d deprived kitten were also studied. The primary effect of both forms of deprivation was to render the system of fourth layer bands more distinct, particularly within the hemisphere contralateral to the eye injection.

Visual area of the lateral suprasylvian gyrus (Clare—Bishop area) of the cat

On anatomical and physiological grounds a zone of cat cortex deep in the medial bank of the suprasylvian sulcus (the Clare—Bishop area) is known to receive strong visual projections both from the lateral geniculate body and area 17. We have mapped receptive fields of single cells in this area in eight cats.