A celebration of the 50th anniversary of David Hubel and Torsten Wiesel's <i>Receptive fields of single neurones in the cat's striate cortex</i>

Abstract

This issue of The Journal of Physiology celebrates the 50th anniversary of the classic joint paper by David Hubel and Torsten Wiesel (Receptive fields of single neurones in the cat's striate cortex, Journal of Physiology 148, 574–591, 1959), which led to a revolution in our understanding of visual processing and to their well-deserved Nobel Prize in 1981. We are delighted to celebrate this publication, for all sorts of good reasons. This was the first joint paper by Hubel & Wiesel, and this and their many subsequent papers helped us to understand not only visual processing, but also how the brain operates. Their papers are not only superb examples of physiological experimentation, but wonderfully clear scientific writing. They explain elsewhere how their paper underwent many drafts and refinements but the key element comes from their own crystal clear logical style. We reproduce the full paper here, not only as a milestone in neurophysiological investigation, but also as a wonderful model for paper writing. The present issue contains fascinating contributions from a wide array of Hubel and Wiesel's collaborators, former postdocs and colleagues. The articles range from research papers to reviews, with reflections and speculations and even philosophical discussions. I should point out that sometimes it is hard to get authors to contribute to Special Issues, but in this case we were overwhelmed with such sheer enthusiasm and delight that our authors jumped at the chance to celebrate David and Torsten. The esteem, genuine affection and considerable respect in which these gentlemen are held is quite moving. They are held thus not only for their considerable scientific achievements, but also for their mentoring of individual colleagues to whole departments. They say that you should never meet your heroes; this is nonsense. I was fortunate enough to meet both of David and Torsten over the last several months and could feel not only the power of their sheer brilliance, but also the warmth, patience, and kindness that the following authors all point out. Many scientists today (sadly) are focused solely on their work or the narrow world of their laboratories or career prospects. David Hubel and Torsten Wiesel have an amazing number of outside interests and achievements and one feels they would have made a considerable impact in whatever they eventually chose as their ‘day job’. On a personal note, I’d like to thank them not only for their immense help in putting this celebratory Special Issue together but also for putting me on the path to a career in physiology. I remember listening to the Reith Lectures on the radio when I was a teenager, and in particular Colin Blakemore's wonderful ‘Mechanics of the Mind’. In one episode (I used to play the cassette tapes over and over; they wore out) Blakemore talked about the experiments of Hubel & Wiesel, and I never quite got over the excitement and shock of hearing about how nerve cells could ‘decode’ bars moving in the animals visual field, indeed discern tiny differences in orientation. When the time came for me to give lectures to first year students, some of whom had done no biology at all, I would always use those beautiful early experiments of David Hubel and Torsten Wiesel to make them see not only how marvelous the brain was, but how with insight, patience and sheer determination, scientists could figure out actually how this marvel comes about. We don't celebrate achievements nearly enough, but I hope you will join with The Journal in celebrating the wonderful achievements and contributions of Hubel and Wiesel; Happy Scientific Birthday gentlemen. D. H. Hubel and T. N. Wiesel The Wilmer Institute, The Johns Hopkins Hospital and University, Baltimore, MD, USA Recordings were made from single cells in the striate cortex of lightly anaesthetized cats. The retinas were stimulated separately or simultaneously with light spots of various sizes and shapes. In the light-adapted state cortical cells were active in the absence of additional light stimulation. Increasing the depth of anaesthesia tended to suppress this maintained activity. Restricted retinal areas which on illumination influenced the firing of single cortical units were called receptive fields. These fields were usually subdivided into mutually antagonistic excitatory and inhibitory regions. A light stimulus (approximately 1 s duration) covering the whole receptive field, or diffuse illumination of the whole retina, was relatively ineffective in driving most units, owing to mutual antagonism between excitatory and inhibitory regions. Excitatory and inhibitory regions, as mapped by stationary stimuli, were arranged within a receptive field in a side-by-side fashion with a central area of one type flanked by antagonistic areas. The centres of receptive fields could be either excitatory or inhibitory. The flanks were often asymmetrical, in that a given stationary stimulus gave unequal responses in corresponding portions of the flanking areas. In a few fields only two regions could be demonstrated, located side by side. Receptive fields could be oriented in a vertical, horizontal or oblique manner. Effective driving of a unit required a stimulus specific in form, size, position and orientation, based on the arrangement of excitatory and inhibitory regions within receptive fields. A spot of light gave greater responses for some directions of movement than for others. Responses were often stronger for one direction of movement than for the opposite; in some units these asymmetries could be interpreted in terms of receptive field arrangements. Of the 45 units studied, 36 were driven from only one eye, 15 from the ipsilateral eye and 21 from the contralateral; the remaining nine could be driven from the two eyes In some units the two eyes were in various of of one eye over the were units were driven from regions in the two unit the fields mapped for the two eyes were in size, and orientation, and when stimulated with moving In a unit excitatory and inhibitory regions of the two receptive fields and and mutual antagonism could be as within a single receptive In the central the visual from to striate cortex an to and single unit responses at several of light most in units at one no be the most at the differences in responses at in the one hope to some understanding of the in visual spots of light on the light-adapted that cells have receptive with an and an or The and areas within a receptive field were to be mutually and a spot to the of the field was than one covering the whole receptive field In the moving light-adapted it was that the of cortical cells gave or no to light covering most of the visual field, spots in a retinal often responses A moving spot of light often stronger responses than a stationary and sometimes a moving spot gave for one direction than for the The present investigation, made in a of receptive fields of cells in the cat's striate Receptive fields of the cells in this paper were into excitatory and inhibitory and areas. In this respect they retinal receptive fields. the and arrangement of excitatory and inhibitory areas from the in retinal was made to responses to moving with receptive field arrangements. cells could be from either eye, and in these was In this of experiments were were anaesthetized with and light anaesthesia was maintained the by additional The eyes were by of the of this made it to use of both eyes were and was by of used with a the from and The were held by A by & was used for and the of the illumination was usually about and the stimulus was Many sizes and of spots of light could be and these were focused on the were of the of 1 a of light was The a covering most of the visual On this light spots of various sizes and were The light was a on an could be the in various directions and with an as as of at the cat's eyes could be but spots were used for receptive fields. of are given in terms of in the 1 on the about were focused on the two retinas with in of the cat's for were by a from to A of was given by a which the whole were by a of retinal illumination corresponding to these & were within the range but were than those with the the two of were from the unit they were to give This of light spots on a was by & to light were on of paper on the in such a as to the responses were excitatory or inhibitory. The of paper of these and the and of the regions. unit was by A was to the by a The cortical was from the to and of the cortex This gave the for of receptive field, which often many were with a and a were used in a Recordings were made from of the from to about the of an was made and at the of the the was first with and with The of the were with and the brain was from the and were made in the of and with These that all units were located in the of the striate between of units in the striate cortex and physiological will not be with in this is that cortical cells and in their firing and in their responses to diffuse light The that the were from is based on these as as on for and & units were in the cat's striate The to be are based on of 45 of of which was for a of from to of this were usually required for of these In with in the moving light-adapted single cortical units in the absence of in retinal was than in moving and from about The was to light on a number of the anaesthesia in a of maintained activity. This not that all cortical cells are active in the absence of light stimuli, many units have In most units it was to a area in the from which firing could be influenced by This area was called the receptive field of the cortical the by for retinal The for out a receptive field is in a 1 spot on the in some areas of the eye a in the maintained with a of when the light was and areas when an in firing and The to the of the of a oriented from which responses were flanked on either side by areas which gave responses The field an area about The had a of 1 and was Responses of a in the cat's striate cortex to a spot of light Receptive field located in the eye to the from which the unit was to and the area to the horizontal from the ipsilateral The of the receptive field is to the areas areas inhibitory of this are on of 1 spot in the of the 1 spot on from spot covering the illumination of stimulus 1 receptive fields could be subdivided into excitatory and inhibitory regions. area was excitatory illumination an in of was inhibitory light maintained and was by an or either of firing or an In many units the of maintained was or to and only an was was, always to inhibitory the firing was first by of excitatory regions. used here, and are both and could be from both regions, either the light stimulus or following We have to receptive field regions to the the is used and not a inhibitory of on the the of firing could also be to a in maintained When excitatory and inhibitory regions in the were stimulated simultaneously they in a mutually antagonistic a than when either was In most fields a stationary spot enough to the whole receptive field was a spot to diffuse light of the at these and stimulus was also In the unit of 1 the inhibitory responses were with a spot of light covering the central The responses a stimulus to the two flanking regions. always within an area of the and the was with a stimulus the of this In the unit of and was in to a 1 spot in the central A in one of the flanking areas and was no to an spot covering the receptive field The unit was by a narrow 1 by oriented over the excitatory In a horizontal of light was the that the central area was of a when stimulated the of the was responses and to a Responses of a unit to with spots of light Receptive field located in area of unit could also be by the ipsilateral 1 spot in the spot to the spot covering receptive and and as in unit as in responses to a light 1 of on of receptive as to of responses to a 1 oriented in various with one always covering the of the receptive that this central responses when stimulated and as in stimulus 1 These be in terms of excitatory and inhibitory areas. The of the to a oriented is by over the excitatory and by the of inhibitory regions. When of the inhibitory flanking areas were by the responses were or a horizontal was ineffective it stimulated a of the central excitatory and portions of the antagonistic regions. units were not enough to of receptive fields with light In these the stimulus could be by the size, and of the stimulus a clear was when a with excitatory or inhibitory responses was the areas in the receptive field could only be an is in two flanking areas are by a in various like the of a always the of the The thus with those with a spot Receptive fields a central area and flanks a but several were fields had narrow central regions with flanking areas had a central area and flanks and In many fields the two flanking regions were asymmetrical, in and in these a given spot gave unequal responses in corresponding regions. In some units only two regions could be one excitatory and the side by side. In these of it is that was a flanking area which could not be the present of horizontal receptive field of eye of at of an excitatory see inhibitory. illumination stimulus 1 This unit was from either eye The between corresponding of the two receptive fields. Receptive field in the eye was located and to area in the ipsilateral eye, and Receptive fields of the two eyes were in and orientation, as in of the The of in the receptive field are to the of and stimulus and as in unit as in horizontal covering flanking of for of covering the flanking regions of the two of horizontal covering both flanking regions of the for of all flanking regions. horizontal in central of for of central regions of both 1 unit as in antagonism between inhibitory in the eye and an excitatory in the stationary horizontal in of horizontal covering flanking of of the regions of 1 and between inhibitory in eye and an excitatory in the moving spot of eye spot from inhibitory in eye, an eye spot into excitatory in eye, an both eyes spot from inhibitory in eye into excitatory of eye, a 1 of a field with only two regions is in The inhibitory was to an area of about 1 The excitatory area to the of the inhibitory was a spot of at was required to a and a was when the excitatory area was the in between excitatory and inhibitory the of the two together and no was The stimulus in was of the position of the between light and was for a A of the to the light to on the inhibitory the to a between light and when and was often an type of Responses only from eye Receptive field outside of area 1 spot covering the inhibitory of a in light spot covering regions in a and and stimulus and as in receptive fields with central and flanking regions have either excitatory or inhibitory and we have no that one is than the from ipsilateral eye only Receptive field to area and excitatory flanking stronger than 1 covering central 1 covering flanking spot covering receptive movement of oriented to of field in for the two directions of and stimulus and as in 1 The of a field was as a to an oriented of the field examples were with oriented or were with respect to the field with respect to the horizontal of the retinas were not of eye have of the these the two fields in were a horizontal field is in and and oblique fields in and from unit by ipsilateral eye to stationary influenced by movement in an area to area A and with as to the responses only one direction was and to the and as in 1 units have had their receptive fields within the of to the in which they were receptive fields were located in or the area were in retinal regions. receptive fields were located in the of the cat's the retinal have also to the was sometimes to the of receptive the were often field on and of the stimulus spot and on as for the by and these and the stimulus fields in from about to in the present no have made of in receptive fields of fields in the unit with the and with were always to be in and a of several units in of This would that within this range was in or of receptive fields. units have in of a light stimulus in the visual field was an of was in the moving 1959), these were sometimes the only by which the firing of a unit could be moving spots of light the in various directions and at of to movement could be in a spots of light were and for of also the of the was for in the unit of moving a and the field a at moving a horizontal and was The excitatory and inhibitory areas one at a time and area could but a horizontal at all the antagonistic regions and was The to a was about the for the two directions of unit as in and Receptive field in Responses to a and the receptive and stimulus as in 1 In some units a could be at of the receptive The receptive field in had an inhibitory flanked by flanking regions. A horizontal or over the receptive field a as excitatory was A of this unit is given in the of this Many units of a type in their responses to In these a oriented responses that were for the two directions of In the of the receptive field of a inhibitory area flanked by two excitatory of which the was than the was and a spot was ineffective A narrow with to that of the field, a when in a direction and to the but only a when and to the A of these on the of within the receptive field will be given in the A number of units to some directions of but not at all to the of this is the unit of a was and in a number of and to the with many units, this one could not be by stationary by moving it was to get some of the receptive field for in this the oblique orientation. units in this could be driven only from one eye, 15 from the eye ipsilateral to the in which the unit was and 21 from the could be driven from the two eyes of these cells could be as from either eye, but often the two eyes were not and of of one eye over the were In these units the receptive fields were always in of the two a unit with a receptive field in the of the area of one eye had a corresponding field in the of the area of the Receptive fields were mapped out on a in of the the eye with the eyes that receptive fields as were usually side by of the receptive fields of a single unit could be mapped out in the two eyes they were in in of their and in of excitatory and inhibitory regions within the The receptive fields in were from a unit in which field was of an inhibitory flanked by narrow horizontal excitatory areas. Responses of the unit to a horizontal the field have in for the between corresponding regions in the receptive fields of the two eyes of two corresponding excitatory areas a which was stronger than when either area was stimulated the excitatory flanks within one receptive field the most was with a stimulus covering the excitatory areas in the two eyes of responses when inhibitory areas in the two eyes were stimulated together could also be between receptive fields of the two eyes the central area of the eye gave an and one flanking area of the eye gave an When stimulated simultaneously the two regions gave no The of and antagonism could thus be between receptive fields of the two and were not to single in this unit it was with a moving stimulus to that areas not always but be mutually The eye was and a spot was on the over the area of the the spot as from the of the eye, an When the eye was and the eye the movement a as the flanking excitatory of the eye was The was with both eyes and a was the movement was made in such a that the from the eye to the from the a greater than with either is that within a single receptive field regions in this in to a moving In this most cells in the striate cortex had receptive fields with excitatory and inhibitory regions. This type of was first by for retinal and also in a of neurones in the & Wiesel, at in the visual a be by one type of stimulus and by a stimulus the two is always retinal and cells give clear responses to a spot of light covering the receptive the cortical the antagonism between excitatory and inhibitory areas to be the of units or no to with in the cortex of moving that this is not a of & only diffuse light were to about the units in the striate cortex, the could not be at In about the units in striate cortex were to be from the and these to diffuse The were to be or their for the most they at all to diffuse The between our and those of and be by the of from the present On the it be that cells to diffuse light are in the cortex than our would but were not by our of and cortical cells not be with of diffuse This would be in with the that in some for of the striate cortex The between retinal cells and cortical cells was to be in the arrangement of excitatory and inhibitory of their receptive fields. are no units in the cortex have had fields with the of retinal the of fields in the cortex have not at of or are the most for retinal and the of the spot is on the of the central area of the receptive field the cortical a spot was often for driving of unit it was to a spot with a particular and orientation. The cortical units have had in a side-by-side of excitatory and inhibitory usually with of one or both of regions. The and of the most light stimulus was given by the of a particular The of stimulus used in these were usually of spots of light and between light and and were to one type of thus not of within that and at the time could areas The of and antagonism within receptive fields to a for the of stimuli, in and orientation. by and units of which for their units in this paper have had receptive fields with excitatory and inhibitory areas. a number of units in the striate cortex could not be solely in these These units with are of receptive fields be in the cortex, the was and be by the We for have to from or from units a maintained would not to be We have the and the of receptive but have not to them into is for of several on to single and for a of on to single cortical cells with these our that some single cortical cells be influenced from relatively retinal regions. These the receptive are subdivided into excitatory and inhibitory some of these be with the of the fields. This is by the fields in and in which the central regions were but and by that of in which both flanks were is also by the field of which had a of about but inhibitory was only about 1 in a unit be influenced from a relatively wide retinal and about a stimulus within that of a stimulus the was to be a of a often than a stationary movement of a usually responses only when the was oriented in a This was sometimes by the arrangement within the receptive fields as mapped out with stationary In many units the responses to movement in directions were when the direction of movement was was no to movement in the direction have with moving spots in the was not always to a for but at the of of flanking areas was with the of responses to in the unit of movement responses were by moving a from the inhibitory to the stronger of the two excitatory regions. it is to movement responses in terms of between excitatory and inhibitory areas. This is in areas antagonistic when with stationary spots could be to be with moving stimuli, and a was when a spot from an to an of responses by of regions to the excitatory area for the in the eye and for cells both in the and in the have for in the and for and in the In it that these are with and in the striate cortex would two the particular within receptive fields of excitatory and inhibitory regions to the form, and of the most stimuli, and these play a in of is clear from of eyes with spots of light that some cortical units are from one eye either the ipsilateral or the be driven by the two In of the number of cells studied, no be as to the of these units and but it that all are of units that the receptive fields mapped out separately in the two eyes were The excitatory and inhibitory areas were located in of the were and and to the direction of When corresponding of the two receptive fields were stimulated that the receptive fields as into the visual field are when an on an unit which be by the one eye should be influenced when both eyes are The two retinal of or in of the point will not on corresponding of the and their should not They or not at is that when an in the visual field the two a on units, those in some to an of the that is which are the from the as the should out in On the such units be to of to with the of We to thank for and and and for their This work was in by and and in by of Scientific and