David H. Hubel

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.

The period of susceptibility to the physiological effects of unilateral eye closure in kittens

1. Kittens were visually deprived by suturing the lids of the right eye for various periods of time at different ages. Recordings were subsequently made from the striate cortex, and responses from the two eyes compared. As previously reported, monocular eye closure during the first few months of life causes a sharp decline in the number of cells that can be influenced by the previously closed eye.

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.

Anatomy and physiology of a color system in the primate visual cortex

Staining for the mitochondrial enzyme cytochrome oxidase reveals an array of dense regions (blobs) in the primate primary visual cortex. They are most obvious in the upper layers, 2 and 3, but can also be seen in layers 4B, 5, and 6, in register with the blobs in layers 2 and 3. We compared cells inside and outside blobs in macaque and squirrel monkeys, looking at their physiological responses and anatomical connections. Cells within blobs did not show orientation selectivity, whereas cells between blobs were highly orientation selective. Receptive fields of blob cells had circular symmetry and were of three main types, Broad-Band Center-Surround, Red-Green Double-Opponent, and Yellow-Blue Double-Opponent. Double-Opponent cells responded poorly or not at all to white light in any form, or to diffuse light at any wavelength. In contrast to blob cells, none of the cells recorded in layer 4C beta were Double-Opponent: like the majority of cells in the parvocellular geniculate layers, they were either Broad-Band or Color- Opponent Center-Surround, e.g., red-on-center green-off-surround. To our surprise cells in layer 4C alpha were orientation selective. In tangential penetrations throughout layers 2 and 3, optium orientation, when plotted against electrode position, formed long, regular, usually linear sequences, which were interrupted but not perturbed by the blobs. Staining area 18 for cytochrome oxidase reveals a series of alternating wide and narrow dense stripes, separated by paler interstripes. After small injections of horseradish peroxidase into area 18, we saw a precise set of connections from the blobs in area 17 to thin stripes in area 18, and from the interblob regions in area 17 to interstripes in area 18. Specific reciprocal connections also ran from thin stripes to blobs and from interstripes to interblobs. We have not yet determined the area 17 connections to thick stripes in area 18. In addition, within area 18 there are stripe-to-stripe and interstripe- to-interstripe intrinsic connections. These results suggest that a system involved in the processing of color information, especially color-spatial interactions, runs parallel to and separate from the orientation-specific system. Color, encoded in three coordinates by the major blob cell types, red-green, yellow-blue, and black-white, can be transformed into the three coordinates, red, green, and blue, of the Retinex algorithm of Land.

THE ROLE OF FIXATIONAL EYE MOVEMENTS IN VISUAL PERCEPTION

Our eyes continually move even while we fix our gaze on an object. Although these fixational eye movements have a magnitude that should make them visible to us, we are unaware of them. If fixational eye movements are counteracted, our visual perception fades completely as a result of neural adaptation. So, our visual system has a built-in paradox — we must fix our gaze to inspect the minute details of our world, but if we were to fixate perfectly, the entire world would fade from view. Owing to their role in counteracting adaptation, fixational eye movements have been studied to elucidate how the brain makes our environment visible. Moreover, because we are not aware of these eye movements, they have been studied to understand the underpinnings of visual awareness. Recent studies of fixational eye movements have focused on determining how visible perception is encoded by neurons in various visual areas of the brain.

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,

Single unit activity in lateral geniculate body and optic tract of unrestrained cats

In two recent studies of the cats striate cortex (Hubel, 1959; Hubel & Wiesel, 1959) single units were shown to react to light stimuli in a highly specific manner. Most units responded either feebly or not at all to stimulation of the retina with diffuse light, but gave brisk responses to stationary or moving restricted spots of light. Responses to moving spots often varied with the direction of movement. It was clear that such responses must be the result of complex integrative mechanisms. The present study was undertaken to find out whether similar responses occur in retinal ganglion cells or cells of the dorsal lateral geniculate body. Lateral geniculate units have not previously been studied with restricted light stimulation, and although the cats retinal ganglion cell has been extensively investigated by Kuffler and his co-workers (Kuffler, 1953; iKuffler, FitzHugh & Barlow, 1957), responses to moving spots were not examined. Thus it has not been possible to say whether the complex activity of cortical units originates in the cortex itself, or at lower levels. Methods for stereotaxic depth recordings in the unanaesthetized unrestrained animal were developed in order to make cortical and depth studies under similar conditions. These techniques make it possible to record from single units from virtually any part of the brain of the freely moving animal.

Microsaccadic eye movements and firing of single cells in the striate cortex of macaque monkeys

When viewing a stationary object, we unconsciously make small, involuntary eye movements or ‘microsaccades’. If displacements of the retinal image are prevented, the image quickly fades from perception. To understand how microsaccades sustain perception, we studied their relationship to the firing of cells in primary visual cortex (V1). We tracked eye movements and recorded from V1 cells as macaque monkeys fixated. When an optimally oriented line was centered over a cells receptive field, activity increased after microsaccades. Moreover, microsaccades were better correlated with bursts of spikes than with either single spikes or instantaneous firing rate. These findings may help explain maintenance of perception during normal visual fixation.

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.