BarlowHB (1982). David Hubel and Torsten Wiesel. Their contribution towards understanding the primary visual cortex. Trends in Neuroscience, 5, 145-152 TINS - May 1982 145 tical neurons, but had reasoned that light flooding the whole visual field, which made the whole field look bright, was the commonsense stimulus to use, to explore cortical neurons. Even at the retina and lat- eral geniculate nucleus (LGN) a uniform field is not nearly as effective as a small David Hubel and Torsten Wiesel point of light because of lateral inhibition, and Hubel and Wiesel therefore explored Their contributions towards understanding the field with small spots in order to map the the primary visual cortex individual receptive fields of their cortical neurons. Examples of these maps are given in Fig. 2. Unlike the receptive fields at H. B. Barlow lower levels in the visual pathway, those of the cortical neurons were found to be elon- gated, and in consequence the patterned stimulus they responded to best was an Last year's Nobel Prize winners in Physiology and Medicine, David Hubel and oriented slit, bar or edge. Hubel himself Torsten Wiesel (see Fig. 1), published a paper 20 years ago that was a landmark in says that they were aided in making this cortical neurophysiology is. And then a year later, in 196314.~.~, they published their important discovery by the accidental first work on the development of the visual pathway in kittens, and this too opened a observation that a fine dark line caused by a completely new field for physiological study. Even by that daze many people felt their crack on one of their slides gave rise to a work was of suffu:ient merit for the prize, and it has been followed by 15 years of much larger response than the black spot outstandingly successful collaboration producing a flow of important new results year that was intended as the stimulus. afier year. By now the award must be considered, not only one of the most Pattern selectivity in single cells was richly-deserved, but also one of the hardest-earned. already known, and the behavioural import- ance of 'fly-detectors' in the frog's retina' Their work on visual cortex started when development, we shall gain a fair idea of was at that time being emphasized by David Hubel joined Torsten Wiesel in what they have achieved. Lettvin and his colleagues at MIT'zr. But Steve Kuffler's laboratory at Johns Hopkins selectivity for orientation was new, and so in 1958. Hubel, working at the Walter Reed Pattern ~dleettvtty of cortical neurons was the fact that all recordable neurons in Research Institute, had developed a method In 1962, many people were not at all the cortex were pattern selective. The of recording from single neurons in the cor- convinced that it would be possible to make implications were revolutionary; instead of tex, whereas Wiesel had been continuing any functional sense of the activity of a thinking of the primary visual cortex (area Steve Kuffler's own work on the retina. single nerve cell in a sensory pathway, let 17) as a structure with myriads of cells each They published their fu-st results on visual alone in the cerebral cortex which contains taking part in forming every visual image. cortex in 195912. soon after Hubel's arrival some 10 s° neurons. The claim they made, one was forced to realize that each cell had in the laboratory, but it was not until 1962, that the appropriate stimulus could be found its own very specific stimulus require- after Kuffler had moved his laboratory to for any single neuron in the primary visual ments, and consequently when it was active Harvard and at least 4 years after the work cortex whose activity they could reliably each cell 'said' something specific about the had started, that the major paper on the cat's detect, therefore had a major impact. nature of the image in its particular region cortex appeared. As far as cortical Others had successfully recorded from cot- of the visual field. neurophysiology was concerned it was the dawn of a new day, for the preceding night had been illuminated chiefly by the murky glow of evoked potentials and electro- encephalography. They reported three main results: first, they believed that neurons in primary visual cortex could always be excited by light if the appropriate patterned stimulus was found; second, the majority of neurons were binocular and could be excited through either eye; and third, they showed that cells of a given type were clustered according to a columnar microstructure. In their developmental work they showed both a high degree of ontogenetic determination of the features of the visual pathway, and striking plasticity resulting from abnormalities of experience. All of these findings were new, and all have been amply confirmed, though with certain qualifications and additions. If we consider these four problems, i.e. pattern selectivity, Fig. I. David Hubel (left) and Torsten Wiesel(right). (Photographwas taken at the Cold Spring Harbor binocularity, columnar microstructure and Symposiumin 1975by Colin Blakemore.) ~ Elsevier Biomedical Press /9~2 LI37~ 5~I2,~2,'(~K~ i~t,$o2 75 BarlowHB (1982). David Hubel and Torsten Wiesel. Their contribution towards understanding the primary visual cortex. Trends in Neuroscience, 5, 145-152 146 17N,S' ,~I.~/~2 Different cells differed from each other in many ways. Some preferred one orienta- A C <~,/4/ O ~ ~9/" tiom some preferred another, and similarly m with the size of the bar, and whether it was w bright or dark, and the direction it was moved in. But there was also a major di~ 8 ,, tinction into two types they called simple and complex. The former is the type shown ~" ~, ~, ~" ,~ ._.~g,¢ 44 < ,d, ,va ~- .p in Fig. 2 and these cells responded to pat- " ~" " terned stimuli in a way that could be roughly predicted from the shape and struc- ture of their receptive fields, as plotted with E a small spot of light turned on and off. "a.~-a,x~n"/~ Others, however, had larger receptive ", fields and often gave both 'on' and 'off "~_.~/a4.~ 4"X4" responses to a small spot over large areas. ~--n ..~ X -r ~" ,z::7 4- "~ / . 4 "~* a',.'/'b these other cells also preferred one orienta- tion, and often one direction of movement, ve~ just like the simple type. They named them 4. complex and suggested that they were acti- Fig. 2. Examples of receptive fields plotted from isolated units in the primary visual cortex of the cat. When a vated by a collection of neurons of the spot oflight was aimed at a position marked by a cross it caused a response when turned on. whereas for a simple type that all shared the property of position marked by a triangle the response occurred when it was turned off Summation occurred when light preferring one particular orientation, as fell simultaneously in regions marked alike, whereas light falling in an oppositely marked region reduced the shown in the lower half of Fig. 3. Since response. The top left fields (11,and B) are from fibres arriving at the cortex from the geniculate. The remainder are from the simple type of cortical neuron, and the response to patterns of light could be they had larger receptive fields they effec- predicted qualitatively from the arrangement of on and off areas of the receptive fields. (This Lt not true for tively generalized the detection of orienta- complex cells.) (FromRef. 13. ) tion over a range of positions; thus, they might provide a rudimentary example of the physiological mechanism lor positional invariance - the ability to recognize the same feature anywhere in the visual field. In later studies they investigated other cortical areas ~ and extended the work to monkeys ~7 as well as cats. This part of their work is a superb example of what might be called the natural history approach to neurophysiology: they observed what their single cells responded best to and classified them, but they made little attempt to ana- lyse the mechanism whereby pattern selec- tivity was achieved, or to fathom the sig- nificance of the types of selectivity F--~--~----/--- / observed. It must be said that their two major suggestions about mechanism have not stood up well. Their idea was that pat- tern selectivity was achieved by summation / from a selected subset of inputs: geniculate afferents from a row ofretinal neurons give I~ ~ ~:i a cortical neuron its orientational prefer- h,i,P' i~lJ~. ~1 ence' they suggested' as sh°wn at the t°P °f [~]~ ~ ~ Fig. 3. It now appears much more likely that inhibition plays the major role in mak- I ing cortical neurons selective~4, just as it I does in retina*, for drugs antagonizing I inhibitory transmitters remove pattern [ ,selectivity. Similarly their suggestion about the hierarchical arrangement of cortical neurons has been undermined by the dis- Fig. 3, The mechanisms for the selectivity of simple and complex cells suggested by Hubel and Wiesel. At the covery of parallel pathways in the visual top tej~ the receptive fields of three retinal ganglion cells are shown. The messages from a large number of system~7, by the demonstration that at least such cells, all lying in a row, are lm~ssed through lateral geniculate neurons and converge on a simple cell. which conSequcntly has a linear receptive field. Below are shown the receptive fields of three dmple type some of the complex cells are directly cortical neurons whose axons converge on a complex cortical neuron. Nowiulays it is recognized thai a excited by geniculate afferentsZ% and by the simple cortical neuron often has very few excitatory geniculate afferents, and that inhibition plays an important discovery of visual patterns that are ineffec- part in their pattern selectivity.