A celebration of the 50th anniversary of David Hubel and Torsten Wiesel's Receptive fields of single...

J Physiol 587.12 (2009) pp 2721–2732 2721

EDITORIAL

A celebration of the 50thanniversary of David Hubel andTorsten Wiesel’s Receptive fieldsof single neurones in the cat’sstriate cortex

Brian RobertsonThe Journal of Physiology, PO Box 502,Cambridge CB1 0AL, UK

Email: [email protected]

This issue of The Journal of Physiologycelebrates the 50th anniversary of the classicjoint paper by David Hubel and TorstenWiesel (Receptive fields of single neuronesin the cat’s striate cortex, Journal of Physio-logy 148, 574–591, 1959), which led to arevolution in our understanding of visualprocessing and to their well-deserved NobelPrize in 1981.

We are delighted to celebrate thispublication, for all sorts of good reasons.This was the first joint paper by Hubel &Wiesel, and this and their many subsequentpapers helped us to understand not onlyvisual processing, but also how the brainoperates. Their papers are not only superbexamples of physiological experimentation,but wonderfully clear scientific writing.They explain elsewhere how their paperunderwent many drafts and refinementsbut the key element comes from their own

crystal clear logical style. We reproduce thefull paper here, not only as a milestone inneurophysiological investigation, but also asa wonderful model for paper writing.

The present issue contains fascinatingcontributions from a wide array of Hubeland Wiesel’s collaborators, former post-docs and colleagues. The articles rangefrom research papers to reviews, withreflections and speculations and evenphilosophical discussions. I should pointout that sometimes it is hard to get authorsto contribute to Special Issues, but in thiscase we were overwhelmed with such sheerenthusiasm and delight that our authorsjumped at the chance to celebrate Davidand Torsten. The esteem, genuine affectionand considerable respect in which thesegentlemen are held is quite moving. Theyare held thus not only for their considerablescientific achievements, but also for theirmentoring of individual colleagues to wholedepartments. They say that you shouldnever meet your heroes; this is nonsense. Iwas fortunate enough to meet both of Davidand Torsten over the last several months andcould feel not only the power of their sheerbrilliance, but also the warmth, patience,and kindness that the following authorsall point out. Many scientists today (sadly)are focused solely on their work or thenarrow world of their laboratories or careerprospects. David Hubel and Torsten Wieselhave an amazing number of outside inter-ests and achievements and one feels they

would have made a considerable impact inwhatever they eventually chose as their ‘dayjob’.

On a personal note, I’d like to thankthem not only for their immense helpin putting this celebratory Special Issuetogether but also for putting me on thepath to a career in physiology. I rememberlistening to the Reith Lectures on the radiowhen I was a teenager, and in particularColin Blakemore’s wonderful ‘Mechanicsof the Mind’. In one episode (I usedto play the cassette tapes over and over;they wore out) Blakemore talked aboutthe experiments of Hubel & Wiesel, andI never quite got over the excitement andshock of hearing about how nerve cellscould ‘decode’ bars moving in the animalsvisual field, indeed discern tiny differencesin orientation. When the time came forme to give lectures to first year students,some of whom had done no biology at all,I would always use those beautiful earlyexperiments of David Hubel and TorstenWiesel to make them see not only howmarvelous the brain was, but how withinsight, patience and sheer determination,scientists could figure out actually how thismarvel comes about. We don’t celebrateachievements nearly enough, but I hope youwill join with The Journal in celebrating thewonderful achievements and contributionsof Hubel and Wiesel; Happy ScientificBirthday gentlemen.

C© 2009 The Author. Journal compilation C© 2009 The Physiological Society DOI: 10.1113/jphysiol.2009.174151

2722 Republication of Hubel & Wiesel (1959) J Physiol 587.12

Republication of The Journal of Physiology (1959) 148, 574–591:Receptive fields of single neurones in the cat’s striatecortex

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. Theretinas 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 retinalareas which on illumination influenced the firing of single cortical units were called receptivefields. These fields were usually subdivided into mutually antagonistic excitatory and inhibitoryregions. A light stimulus (approximately 1 s duration) covering the whole receptive field, ordiffuse illumination of the whole retina, was relatively ineffective in driving most units, owingto mutual antagonism between excitatory and inhibitory regions. Excitatory and inhibitoryregions, as mapped by stationary stimuli, were arranged within a receptive field in a side-by-sidefashion with a central area of one type flanked by antagonistic areas. The centres of receptivefields could be either excitatory or inhibitory. The flanks were often asymmetrical, in that a givenstationary stimulus gave unequal responses in corresponding portions of the flanking areas. Ina few fields only two regions could be demonstrated, located side by side. Receptive fields couldbe oriented in a vertical, horizontal or oblique manner. Effective driving of a unit required astimulus specific in form, size, position and orientation, based on the arrangement of excitatoryand inhibitory regions within receptive fields. A spot of light gave greater responses for somedirections of movement than for others. Responses were often stronger for one direction ofmovement than for the opposite; in some units these asymmetries could be interpreted in termsof receptive field arrangements. Of the 45 units studied, 36 were driven from only one eye, 15from the ipsilateral eye and 21 from the contralateral; the remaining nine could be driven fromthe two eyes independently. In some binocular units the two eyes were equally effective; in othersvarious degrees of dominance of one eye over the other were seen. Binocularly activated unitswere driven from roughly homologous regions in the two retinas. For each unit the fields mappedfor the two eyes were similar in size, form and orientation, and when stimulated with movingspots, showed similar directional preferences. In a binocular unit excitatory and inhibitoryregions of the two receptive fields interacted, and summation and mutual antagonism could beshown just as within a single receptive field.

In the central nervous system the visual pathway fromretina to striate cortex provides an opportunity to observeand compare single unit responses at several distinct levels.Patterns of light stimuli most effective in influencing unitsat one level may no longer be the most effective at the next.From differences in responses at successive stages in thepathway one may hope to gain some understanding of thepart each stage plays in visual perception.

By shining small spots of light on the light-adaptedcat retina Kuffler (1953) showed that ganglion cells haveconcentric receptive fields, with an ‘on’ centre and an ‘off’periphery, or vice versa. The ‘on’ and ‘off’ areas within a

receptive field were found to be mutually antagonistic, anda spot restricted to the centre of the field was more effectivethan one covering the whole receptive field (Barlow et al.1957). In the freely moving light-adapted cat it was foundthat the great majority of cortical cells studied gave little orno response to light stimuli covering most of the animal’svisual field, whereas small spots shone in a restricted retinalregion often evoked brisk responses (Hubel, 1959). Amoving spot of light often produced stronger responsesthan a stationary one, and sometimes a moving spotgave more activation for one direction than for theopposite.

C© 2009 The Author. Journal compilation C© 2009 The Physiological Society

J Physiol 587.12 Republication of Hubel & Wiesel (1959) 2723

The present investigation, made in acute preparations,includes a study of receptive fields of cells in the cat’sstriate cortex. Receptive fields of the cells consideredin this paper were divided into separate excitatory andinhibitory (‘on’ and ‘off’) areas. In this respect theyresembled retinal ganglion-cell receptive fields. However,the shape and arrangement of excitatory and inhibitoryareas differed strikingly from the concentric patternfound in retinal ganglion cells. An attempt was madeto correlate responses to moving stimuli with receptivefield arrangements. Some cells could be activated fromeither eye, and in these binocular interaction wasstudied.

Methods

In this series of experiments 24 cats were used. Animalswere anaesthetized with intraperitoneal thiopental sodium(40 mg kg−1) and light anaesthesia was maintainedthroughout the experiment by additional intraperitonealinjections. The eyes were immobilized by continuousintravenous injection of succinylcholine; the employmentof this muscle relaxant made it necessary to useartificial respiration. Pupils of both eyes were dilated andaccommodation was relaxed by means of 1% atropine.Contact lenses used with a suitably buffered solution pre-vented the corneal surfaces from drying and becomingcloudy. The lids were held apart by simple wire clips.

A multibeam ophthalmoscope designed by Talbot &Kuffler (1952) was used for stimulation and viewing theretina of the left eye. Background illumination was usuallyabout 0.17 log metre candles (m.c.), and the strongestavailable stimulus was 1.65 log m.c. Many sizes and shapesof spots of light could be produced, and these were wellfocused on the retina. Stimulus durations were of the orderof 1 s.

For binocular studies a different method of lightstimulation was used. The animal faced a large screencovering most of the visual field. On this screen lightspots of various sizes and shapes were projected. Thelight source was a tungsten filament projector mountedon an adjustable tripod. Stimuli could be moved acrossthe screen in various directions and with different speeds.Spots subtending an angle as small as 12 min of arc atthe cat’s eyes could be obtained, but generally 0.5–1 degspots were used for mapping receptive fields. (Dimensionsof stimuli are given in terms of equivalent externalangles; in the cat 1 mm on the retina subtends about4 deg.) Spots were focused on the two retinas with lensesmounted in front of the cat’s eyes. Lenses for focusing wereselected by using a retinoscope. Spot intensities rangedfrom −0.76 to 0.69 log cd m−2. A background illuminanceof −19 log cd m−2 was given by a tungsten bulb whichilluminated the whole screen diffusely. Intensities were

measured by a Macbeth Illuminometer. Values of retinalillumination corresponding to these intensities (Talbot &Kuffler, 1952, Fig. 4) were within the photopic range butwere lower than those employed with the ophthalmoscope.Whenever the two methods of stimulation were checkedagainst each other while recording from the same unitthey were found to give similar results. This principle ofprojecting light spots on a screen was described by Talbot& Marshall (1941). Areas responsive to light were markedon sheets of paper fixed on the screen, in such a wayas to indicate whether the responses were excitatory orinhibitory. The sheets of paper then provided permanentrecords of these responses, and showed the shape, size andorientation of the regions.

Single unit activity was recorded extracellularlyby techniques described previously (Hubel, 1959). Ahydraulic micro-electrode positioner was attached to theanimal’s skull by a rigidly implanted plastic peg. Thecortical surface was closed off from the atmosphere tominimize respiratory and vascular movements of thecortex (Davies, 1956). This method gave the stabilityneeded for thorough exploration of each receptive field,which often took many hours. Electrodes were electro-lytically sharpened tungsten wires insulated with avinyl lacquer (Hubel, 1957). Cathode follower inputand a condenser-coupled pre-amplifier were used in aconventional recording system.

Recordings were made from parts of the lateral gyrusextending from its posterior limit to about Horsley-Clarkefrontal plane 10. At the end of each penetration an electro-lytic lesion was made (Hubel, 1959) and at the endof the experiment the animal was perfused, first withnormal saline and then with 10% formalin. The bordersof the trephine hole were marked with Indian ink dotsand the brain was removed from the skull and photo-graphed. Paraffin serial sections were made in the region ofpenetration and stained with cresyl violet. These sectionsshowed that all units described were located in the greymatter of the striate cortex. Correlation between locationof units in the striate cortex and physiological findings willnot be dealt with in this paper.

There is evidence that cortical cells and afferent fibresdiffer in their firing patterns and in their responses todiffuse light (Hubel, 1960). The assumption that thespikes recorded were from cell bodies is based on thesedifferences, as well as on electrophysiologic criteria fordistinguishing cell-body and fibre spikes (Frank & Fuortes,1955; Hubel, 1960).

Results

Several hundred units were recorded in the cat’s striatecortex. The findings to be described are based on thoroughstudies of 45 of these, each of which was observed for a



period of from 2 to 9 h. Times of this order were usuallyrequired for adequate analysis of these units.

In agreement with previous findings in the freelymoving light-adapted cat (Hubel, 1959) single corticalunits showed impulse activity in the absence of changesin retinal illumination. Maintained activity was generallyless than in freely moving animals, and ranged fromabout 0.1–10 impulses s−1. The low rate was possibly dueto light barbiturate anaesthesia, since on a number ofoccasions deepening the anaesthesia resulted in a decreaseof maintained activity. This need not mean that all corticalcells are active in the absence of light stimuli, since manyquiescent units may have gone unnoticed.

In most units it was possible to find a restricted areain the retina from which firing could be influenced bylight. This area was called the receptive field of the corticalunit, applying the concept introduced by Hartline (1938)for retinal ganglion cells. The procedure for mapping outa receptive field is illustrated in Fig. 1. Shining a 1 degspot (250 μm on the retina) in some areas of the contra-lateral eye produced a decrease in the maintained activity,with a burst of impulses when the light was turned off(Fig. 1a, b and d). Other areas when illuminated producedan increase in firing (Fig. 1c and e). The complete map,illustrated to the right of the figure, consisted of along, narrow, vertically oriented region from which ‘off’responses were obtained (triangles), flanked on eitherside by areas which gave ‘on’ responses (crosses). Theentire field covered an area subtending about 4 deg. Theelongated ‘off’ region had a width of 1 deg and was 4 deglong.

Most receptive fields could be subdivided into excitatoryand inhibitory regions. An area was termed excitatory if

Figure 1. Responses of a cell in the cat’sstriate cortex to a l deg spot of lightReceptive field located in the eye contralateralto the hemisphere from which the unit wasrecorded, close to and below the area centralis,just nasal to the horizontal meridian. Noresponse evoked from the ipsilateral eye. Thecomplete map of the receptive field is shown tothe right. ×, areas giving excitation; �, areasgiving inhibitory effects. Scale, 4 deg. Axes ofthis diagram are reproduced on left of eachrecord. a, 1 deg (0.25 mm) spot shone in thecentre of the field; b–e, 1 deg spot shone onfour points equidistant from centre; f , 5 degspot covering the entire field. Backgroundillumination 0.17 log m.c. Stimulus intensity1.65 log m.c. Duration of each stimulus 1 s.Positive deflexions upward.

illumination produced an increase in frequency of firing.It was termed inhibitory if light stimulation suppressedmaintained activity and was followed by an ‘off’ discharge,or if either suppression of firing or an ‘off’ dischargeoccurred alone. In many units the rate of maintainedactivity was too slow or irregular to demonstrate inhibitionduring illumination, and only an ‘off’ discharge was seen.It was, however, always possible to demonstrate inhibitoryeffects if the firing rate was first increased by stimulationof excitatory regions.

As used here, ‘excitatory’ and ‘inhibitory’ are arbitraryterms, since both inhibition and excitation could generallybe demonstrated from both regions, either during thelight stimulus or following it. We have chosen to denotereceptive field regions according to effects seen duringthe stimulus. Furthermore, the word ‘inhibition’ is useddescriptively, and need not imply a direct inhibitoryeffect of synaptic endings on the cell observed, since thesuppression of firing observed could also be due to adecrease in maintained synaptic excitation.

When excitatory and inhibitory regions (used inthe sense defined) were stimulated simultaneously theyinteracted in a mutually antagonistic manner, giving aweaker response than when either region was illuminatedalone. In most fields a stationary spot large enough toinclude the whole receptive field was entirely without effect(Fig. 1f ). Whenever a large spot failed to evoke responses,diffuse light stimulation of the entire retina at theseintensities and stimulus durations was also ineffective.

In the unit of Fig. 1 the strongest inhibitory responseswere obtained with a vertical slit-shaped spot of lightcovering the central area. The greatest ‘on’ responsesaccompanied a stimulus confined to the two flanking



Figure 2. Responses of a unit tostimulation with circular spots of lightReceptive field located in area centralis ofcontralateral eye. (This unit could also beactivated by the ipsilateral eye.) a, 1 deg spot inthe centre region; b, same spot displaced 3 degto the right; c, 8 deg spot covering entirereceptive field. Stimulus and backgroundintensities and conventions as in Fig. 1. Scale,6 deg.

regions. Summation always occurred within an area ofthe same type, and the strongest response was obtainedwith a stimulus having the approximate shape of thisarea.

In the unit of Figs 2 and 3 there was weak excitation inresponse to a circular 1 deg spot in the central region. Aweak ‘off’ response followed stimulation in one of theflanking areas (Fig. 2a and b). There was no responseto an 8 deg spot covering the entire receptive field(Fig. 2c). The same unit was strongly activated by a narrowslit-shaped stimulus, measuring 1 deg by 8 deg, orientedvertically over the excitatory region (Fig. 3A). In contrast,a horizontal slit of light was completely ineffective, despitethe fact that the central area was capable of evoking aresponse when stimulated alone (Fig. 2a). As the optimum

Figure 3Same unit as in Fig. 2. A, responses to shining arectangular light spot, 1 deg × 8 deg; centre ofslit superimposed on centre of receptive field;successive stimuli rotated clockwise, as shownto left of figure. B, responses to a 1 deg ×5 deg slit oriented in various directions, withone end always covering the centre of thereceptive field: note that this central regionevoked responses when stimulated alone(Fig. 2a). Stimulus and background intensitiesas in Fig. 1; stimulus duration 1 s.

(vertical) orientation of the slit was approached responsesappeared and rapidly increased to a maximum.

These findings can be readily understood in terms ofinteracting excitatory and inhibitory areas. The strengthof the response to a vertically oriented slit is explainedby summation over the excitatory region and by theexclusion of inhibitory regions. When parts of theinhibitory flanking areas were included by rotating the slit,responses were reduced or abolished. Thus a horizontalslit was ineffective because it stimulated a small portionof the central excitatory area, and larger portions of theantagonistic regions.

Some units were not responsive enough to permitmapping of receptive fields with small light spots. Inthese the effective stimulus pattern could be found by



changing the size, shape and orientation of the stimulusuntil a clear response was evoked. Often when a regionwith excitatory or inhibitory responses was establishedthe neighbouring opposing areas in the receptive fieldcould only be demonstrated indirectly. Such an indirectmethod is illustrated in Fig. 3B, where two flanking areasare indicated by using a short slit in various positions likethe hand of a clock, always including the very centre ofthe field. The findings thus agree qualitatively with thoseobtained with a small spot (Fig. 2a).

Receptive fields having a central area and opposingflanks represented a common pattern, but severalvariations were seen. Some fields had long narrow centralregions with extensive flanking areas (Figs 1–3): others hada large central area and concentrated slit-shaped flanks(Figs 6, 9 and 10). In many fields the two flanking regionswere asymmetrical, differing in size and shape; in thesea given spot gave unequal responses in symmetricallycorresponding regions. In some units only two regionscould be found, one excitatory and the other inhibitory,lying side by side. In these cases of extreme asymmetry itis possible that there was a second weak flanking areawhich could not be demonstrated under the presentexperimental conditions.

An interesting example of a field with only two opposingregions is shown in Fig. 4. The concentrated inhibitoryregion was confined to an area of about 1 deg (Fig. 4a).The excitatory area situated to the right of the inhibitorywas much larger: a spot of at least 4 deg was required toevoke a response, and a very strong discharge was seenwhen the entire 12 deg excitatory area was illuminated(Fig. 4b). Despite the difference in size between excitatoryand inhibitory areas, the effects of stimulating the twotogether cancelled each other and no response was evoked(Fig. 4c). The semicircular stimulus in Fig. 4b was ofspecial interest because the exact position of the verticalborderline between light and darkness was very criticalfor a strong response. A slight shift of the boundary tothe left, allowing light to infringe on the inhibitory area,completely cancelled the response to illumination. Sucha boundary between light and darkness, when properly

Figure 4. Responses evoked only fromcontralateral eyeReceptive field just outside nasal border of areacentralis. a, 1 deg spot covering the inhibitoryregion; b, right half of a circle 12 deg indiameter; c, light spot covering regionsilluminated in a and b. Background andstimulus intensities and conventions as inFig. 1. Scale, 12 deg.

positioned and oriented, was often an effective type ofstimulus.

Cortical receptive fields with central and flankingregions may have either excitatory (Fig. 2) or inhibitory(Figs 1, 6 and 7) centres. So far we have no indication thatone is more common than the other.

The axis of a field was defined as a line through its centre,parallel to an optimally oriented elongated stimulus. Foreach of the field types described examples were foundwith axes oriented vertically, horizontally or obliquely.Orientations were determined with respect to the animal’sskull. Exact field orientations with respect to the horizontalmeridians of the retinas were not known, since relaxationof eye muscles may have caused slight rotation of theeyeballs. Within these limitations the two fields illustratedin Figs 1–3 were vertically arranged: a horizontal field isshown in Figs 6, 9 and 10, and oblique fields in Figs 7 and8.

All units have had their receptive fields entirely withinthe half-field of vision contralateral to the hemispherein which they were located. Some receptive fields werelocated in or near the area centralis, while others were inperipheral retinal regions. All receptive fields were locatedin the highly reflecting part of the cat’s retina containingthe tapetum. So far, retinal ganglion cell studies have alsobeen confined to the tapetal region (Kuffler, 1953).

It was sometimes difficult to establish the total sizeof receptive fields, since the outer borders were oftenpoorly defined. Furthermore, field size may depend onintensity and size of the stimulus spot and on backgroundillumination, as has been shown for the retina by Hartline(1938) and Kuffler (1953). Within these limitations, andunder the stimulus conditions specified, fields ranged intotal size from about 4 deg to 10 deg. Although in thepresent investigation no systematic studies have been madeof changes in receptive fields under different conditionsof stimulation, fields obtained in the same unit withthe ophthalmoscope and with projection techniques werealways found to be similar in size and structure, despitea difference of several logarithmic units in intensityof illumination. This would suggest that within this



Figure 5Same unit as in Figs 2 and 3. Receptive fieldshown in Fig. 2. Responses to a slit (1 deg ×8 deg) moved transversely back and forthacross the receptive field. a, slit movedhorizontally. b, slit moved vertically. Backgroundand stimulus intensities as in Fig. 1; time, 1 s.

photopic range there was little change in size ororganization of receptive fields. No units have been studiedin states of dark adaptation.

Responses to movement

Moving a light stimulus in the visual field was generally aneffective way of activating units. As was previously foundin the freely moving animal (Hubel, 1959), these stimuliwere sometimes the only means by which the firing of aunit could be influenced. By moving spots of light acrossthe retina in various directions and at different speedspatterns of response to movement could be outlined in aqualitative way.

Slit-shaped spots of light were very effective and usefulfor studies of movement. Here also the orientation of theslit was critical for evoking responses. For example, in theunit of Fig. 3 moving a vertical slit back and forth across thefield evoked a definite response at each crossing (Fig. 5a),whereas moving a horizontal slit up and down was withouteffect (Fig. 5b). The vertical slit crossed excitatory andinhibitory areas one at a time and each area could exertits effect unopposed, but a horizontal slit at all timescovered the antagonistic regions simultaneously, and wastherefore ineffective. The response to a vertical slit movedhorizontally was about the same for the two directions ofmovement.

In some units a double response could be observed ateach crossing of the receptive field. The receptive fieldin Fig. 6 had an extensive inhibitory centre flanked byelongated, horizontally oriented, concentrated flankingregions. A horizontal slit moved slowly up or down overthe receptive field evoked a discharge as each excitatory

Figure 6. Slow up-and-down movementsof horizontal slit (1 deg × 8 deg) acrossreceptive field of left eyeBurst of impulses at each crossing of anexcitatory region. For details see Fig. 9. ×,excitatory; �, inhibitory. Backgroundillumination −1.9 cd m−2; stimulus intensity0.69 cd m−2; time, 1 s.

region was crossed. A further description of this unit isgiven in the binocular section of this paper.

Many units showed directional selectivity of a differenttype in their responses to movement. In these a slit orientedoptimally produced responses that were consistentlydifferent for the two directions of transverse movement.In the example of Fig. 7, the receptive field consisted of astrong inhibitory area flanked by two excitatory areas, ofwhich the right was weaker than the left. Each region waselongated and obliquely oriented. As usual, a large spotwas ineffective (Fig. 7c). A narrow slit, with its long axisparallel to that of the field, produced a strong responsewhen moved transversely in a direction down and to theleft, but only a feeble response when moved up and to theright (Fig. 7d). A tentative interpretation of these findingson the basis of asymmetry within the receptive field willbe given in the Discussion.

A number of units responded well to some directionsof movement, but not at all to the reverse directions.An example of this is the unit of Fig. 8. Again a slitwas moved back and forth transversely in a number ofdifferent directions. Only movements up and to the rightevoked responses. As with many units, this one could notbe activated by stationary stimuli; nevertheless, by usingmoving stimuli it was possible to get some idea of thereceptive field organization – for example, in this unit, theoblique orientation.

Binocular interaction

Thirty-six units in this study could be driven only fromone eye, 15 from the eye ipsilateral to the hemisphere



Figure 7. Unit activated from ipsilateraleye onlyReceptive field just temporal to area centralis.Field elongated and obliquely oriented. Leftexcitatory flanking region stronger than right.a, 1 deg × 10 deg slit covering central region;b, 1 deg × 10 deg slit covering left flankingregion; c, 12 deg spot covering entire receptivefield; d, transverse movement of slit (1 deg ×10 deg) oriented parallel to axis of field – notedifference in response for the two directions ofmovement. Background and stimulusintensities and conventions as in Fig. 6. Scale,10 deg; time, 1 s.

in which the unit was situated, and 21 from the contra-lateral. Nine, however, could be driven from the two eyesindependently. Some of these cells could be activated justas well from either eye, but often the two eyes were notequally effective, and different degrees of dominance ofone eye over the other were seen. In these binocular unitsthe receptive fields were always in roughly homologousparts of the two retinas. For example, a unit with a receptivefield in the nasal part of the area centralis of one eye hada corresponding field in the temporal part of the areacentralis of the other eye.

Receptive fields were mapped out on a screen in front ofthe cat. With the eye muscles relaxed with succinylcholinethe eyes diverged slightly, so that receptive fields as chartedwere usually side by side, instead of being superimposed.Whenever the receptive fields of a single unit could bemapped out in the two eyes separately, they were similarin shape, in orientation of their axes, and in arrangementsof excitatory and inhibitory regions within the field.

The receptive fields shown in Fig. 9 were obtainedfrom a binocularly activated unit in which each fieldwas composed of an inhibitory centre flanked by narrowhorizontal excitatory areas. Responses of the same unit toa horizontal slit moved across the field have already beenshown in Fig. 6, for the left eye.

Summation occurred between corresponding regionsin the receptive fields of the two eyes (Fig. 9). Thussimultaneous stimulation of two corresponding excitatoryareas produced a response which was clearly stronger thanwhen either area was stimulated alone (Fig. 9A). As theexcitatory flanks within one receptive field summed, themost powerful response was obtained with a stimuluscovering the four excitatory areas in the two eyes (Fig. 9B).Similarly, summation of ‘off’ responses occurred wheninhibitory areas in the two eyes were stimulated together(Fig. 9C).

Antagonism could also be shown between receptivefields of the two eyes (Fig. 10A). Stimulated alone thecentral area of the left eye gave an ‘off’ response, and

one flanking area of the right eye gave an ‘on’ response.When stimulated simultaneously the two regions gave noresponse. The principles of summation and antagonismcould thus be demonstrated between receptive fields ofthe two eyes, and were not limited to single eyes.

Figure 8. Records from unit activated by ipsilateral eye only;unresponsive to stationary spots, influenced by movement inan area temporal to area centralisA slit (0.5 deg × 8 deg) moved back and forth transversely withdifferent orientations, as shown to the left. For slit orientationsevoking responses only one direction was effective – up and to theright. Stimulus and background intensities as in Fig. 6; time, 1 s.



Figure 9This unit was activated from either eye independently. The illustration shows summation between correspondingparts of the two receptive fields. Receptive field in the contralateral eye was located just above and nasal to areacentralis; in the ipsilateral eye, above and temporal. Receptive fields of the two eyes were similar in form andorientation, as shown in upper right of the figure; scale 8 deg. The pairs of axes in the receptive field diagram arereproduced to the left of each record. Background and stimulus intensities and conventions as in Fig. 6. (Sameunit as in Fig. 6.) A, 1, horizontal slit covering lower flanking region of right eye; 2, same for left eye; 3, pair of slitscovering the lower flanking regions of the two eyes. B, 1, pair of horizontal slits covering both flanking regions ofthe right eye; 2, same for left eye; 3, simultaneous stimulation of all four flanking regions. C, 1, horizontal slit incentral region of right eye; 2, same for left eye; 3, simultaneous stimulation of central regions of both eyes. Time,1 s.

Finally, in this unit it was possible with a movingstimulus to show that opposite-type areas need not alwaysinhibit each other (Fig. 10A), but may under certaincircumstances be mutually reinforcing (Fig. 10B). Theright eye was covered, and a spot was projected on thescreen, over the centre (inhibitory) area of the left eye.Moving the spot as illustrated, away from the centre regionof the left eye, produced an ‘off’ response (Fig. 10B, 1).When the left eye was covered and the right eye uncovered,making the same movement again evoked a response as the

Figure 10Same unit as in Fig. 9. A, antagonism between inhibitory region in the left eye and an excitatory region in theright eye; stationary spots. 1, horizontal slit in centre of left eye; 2, horizontal slit covering upper flanking region ofright eye; 3, simultaneous stimulation of the regions of 1 and 2. B, synergism between inhibitory region in left eyeand an excitatory region in the right eye; moving spot of light. 1, right eye covered, spot moved from inhibitoryregion in left eye, producing an ‘off’ response; 2, left eye covered, spot moved into excitatory region in right eye,producing an ‘on’ response; 3, both eyes uncovered, spot moved from inhibitory region in left eye into excitatoryregion of right eye, producing a greatly enhanced response. Time, 1 s.

flanking excitatory region of the right eye was illuminated(Fig. 10B, 2). The procedure was now repeated with botheyes uncovered, and a greatly increased response wasproduced (Fig. 10B, 3). Here the movement was madein such a way that the ‘off’ response from the left eyeapparently added to the ‘on’ response from the right,producing a response much greater than with either regionalone. It is very likely that within a single receptive fieldopposite-type regions may act in this synergistic way inresponse to a moving stimulus.



Discussion

In this study most cells in the striate cortex had receptivefields with separate excitatory and inhibitory regions.This general type of organization was first described byKuffler (1953) for retinal ganglion cells, and has alsobeen found in a preliminary study of neurones in thelateral geniculate body (Hubel & Wiesel, unpublished).Thus at three different levels in the visual system a cellcan be inhibited by one type of stimulus and excited byanother type, while a stimulus combining the two is alwaysless effective. Most retinal ganglion and geniculate cellsgive clear responses to a large spot of light covering theentire receptive field. At the cortical level the antagonismbetween excitatory and inhibitory areas appears to bemore pronounced, since the majority of units showed littleor no response to stimulation with large spots. Similarfindings in the cortex of unanaesthetized, freely movingcats (Hubel, 1959) suggest that this is probably not a resultof anaesthesia.

Other workers (Jung, 1953, 1958; Jung & Baumgartner,1955), using only diffuse light stimulation, were able todrive about half the units in the cat striate cortex, whilethe remainder could not be activated at all. In recentstudies (Hubel, 1960) about half the units recorded instriate cortex were shown to be afferent fibres from thelateral geniculate nucleus, and these responded to diffuseillumination. The remainder were thought to be cell bodiesor their axons; for the most part they responded poorly ifat all to diffuse light. The apparent discrepancy betweenour findings and those of Jung and his co-workers mayperhaps be explained by the exclusion of afferent fibresfrom the present studies. On the other hand it may be thatcells responsive to diffuse light flashes are more commonin the cortex than our results would imply, but were notdetected by our methods of recording and stimulating.However, cortical cells may not be primarily concernedwith levels of diffuse illumination. This would be in accordwith the finding that in cats some capacity for brightnessdiscrimination persists after bilateral ablation of the striatecortex (Smith, 1937).

The main difference between retinal ganglion cells andcortical cells was to be found in the detailed arrangementof excitatory and inhibitory parts of their receptive fields. Ifafferent fibres are excluded, no units so far recorded in thecortex have had fields with the concentric configurationso typical of retinal ganglion cells. Moreover, the typesof fields found in the cortex have not been seen at lowerlevels.

Spots of more or less circular (or annular) form are themost effective stimuli for activating retinal ganglion cells,and the diameter of the optimum spot is dependent onthe size of the central area of the receptive field (Barlowet al. 1957). At the cortical level a circular spot was oftenineffective; for best driving of each unit it was necessary

to find a spot with a particular form and orientation.The cortical units described here have had in commona side-by-side distribution of excitatory and inhibitoryareas, usually with marked elongation of one or both typesof regions. The form and size of the most effective lightstimulus was given by the shape of a particular region. Theforms of stimulus used in these studies were usually simple,consisting of slit-shaped spots of light and boundariesbetween light and darkness. Position and orientation werecritical, since imperfectly placed forms failed to cover onetype of region completely, thus not taking advantage ofsummation within that region, and at the same time couldinvade neighbouring, opposing areas (Fig. 3).

The phenomena of summation and antagonism withinreceptive fields seem to provide a basis for the specificityof stimuli, in shape, size and orientation. Units activatedby slits and boundaries may converge upon units ofhigher order which require still more complex stimuli fortheir activation. Most units presented in this paper havehad receptive fields with clearly separable excitatory andinhibitory areas. However, a number of units recorded inthe striate cortex could not be understood solely in theseterms. These units with more complex properties are nowunder study.

Other types of receptive fields may yet be found in thecortex, since the sampling (45 units) was small, and maywell be biased by the micro-electrode techniques. We may,for example, have failed to record from smaller cells, orfrom units which, lacking a maintained activity, wouldtend not to be detected. We have therefore emphasized thecommon features and the variety of receptive fields, buthave not attempted to classify them into separate groups.

There is anatomical evidence for convergence of severaloptic tract fibres on to single geniculate neurons (O’Leary,1940) and for a more extensive convergence of radiationfibres on to single cortical cells (O’Leary, 1941). Consistentwith these anatomical findings, our results show that somesingle cortical cells can be influenced from relatively largeretinal regions. These large areas, the receptive fields, aresubdivided into excitatory and inhibitory regions; somedimensions of these may be very small compared withthe size of the entire fields. This is illustrated by the fieldsshown in Figs 1, 2 and 7, in which the central regions werelong but very narrow; and by that of Fig. 9, in which bothflanks were narrow. It is also shown by the field of Fig. 4,which had a total size of about 12 deg but whose inhibitoryregion was only about 1 deg in diameter. Thus a unit maybe influenced from a relatively wide retinal region and stillconvey precise information about a stimulus within thatregion.

Movement of a stimulus across the retina was foundto be a very potent way of activating a cell, often moreso than a stationary spot. Transverse movement of a slitusually produced responses only when the slit was orientedin a certain direction. This was sometimes explained by



the arrangement within the receptive fields as mapped outwith stationary stimuli (Fig. 5).

In many units (Fig. 7) the responses to movement inopposite directions were strikingly different. Occasionallywhen the optimum direction of movement wasestablished, there was no response to movement inthe opposite direction (Fig. 8). Similar effects havebeen observed with horizontally moving spots in theunanaesthetized animal (Hubel, 1959). It was not alwayspossible to find a simple explanation for this, but at timesthe asymmetry of strength of flanking areas was consistentwith the directional specificity of responses to movement.Thus in the unit of Fig. 7 best movement responseswere found by moving a slit from the inhibitory to thestronger of the two excitatory regions. Here it is possibleto interpret movement responses in terms of synergismbetween excitatory and inhibitory areas. This is furtherdemonstrated in Fig. 10B, where areas antagonistic whentested with stationary spots (Fig. 10A) could be shown tobe synergistic with moving stimuli, and a strong responsewas evoked when a spot moved from an ‘off’ to an ‘on’area.

Inhibition of unitary responses by stimulation ofregions adjacent to the excitatory area has been describedfor the eccentric cell in the Limulus eye (Hartline, 1949)and for ganglion cells both in the frog retina (Barlow,1953) and in the cat retina (Kuffler, 1953). Analogousphenomena have been noted for tones in the auditorysystem (dorsal cochlear nucleus, Galambos, 1944) andfor touch and pressure in the somatosensory system(Mountcastle, 1957). In each system it has been proposedthat these mechanisms are concerned with enhancingcontrast and increasing sensory discrimination. Ourfindings in the striate cortex would suggest two furtherpossible functions. First, the particular arrangementswithin receptive fields of excitatory and inhibitory regionsseem to determine the form, size and orientation of themost effective stimuli, and secondly, these arrangementsmay play a part in perception of movement.

It is clear from stimulation of separate eyes with spotsof light that some cortical units are activated from oneeye only, either the ipsilateral or the contralateral, whileothers can be driven by the two eyes. In view of the smallnumber of cells studied, no conclusion can be drawn as tothe relative proportions of these units (ipsilaterally, contra-laterally and bilaterally driven), but it appears that all threetypes are well represented.

Studies of binocularly activated units showed that thereceptive fields mapped out separately in the two eyes werealike. The excitatory and inhibitory areas were located inhomologous parts of the retinas, were similarly shaped andoriented, and responded optimally to the same directionof movement. When corresponding parts of the tworeceptive fields were stimulated summation occurred (Fig.9). Assuming that the receptive fields as projected into the

animal’s visual field are exactly superimposed when ananimal fixes on an object, any binocularly activated unitwhich can be affected by the object through one eye aloneshould be much more strongly influenced when both eyesare used. The two retinal images of objects behind or infront of the point fixed will not fall on correspondingparts of the fields, and their effects should therefore notnecessarily sum. They may instead antagonize each otheror not interact at all.

It is possible that when an object in the visual field exerts,through the two eyes, a strong influence on binocularlyactivated units, those influences may lead in some way toan increased awareness of the object. If that is so, thenobjects which are the same distance from the animalas the object fixed should stand out in relief. On theother hand such units may be related to mechanisms ofbinocular fixation, perhaps projecting to mid-brain nucleiconcerned with the regulation of convergence.

References

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Barlow HB, FitzHugh R & Kuffler SW (1957). Change oforganization in the receptive fields of the cat’s retina duringdark adaptation. J Physiol 137, 338–354.

Davies PW (1956). Chamber for microelectrode studies in thecerebral cortex. Science 124, 179–180.

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O’Leary JL (1940). A structural analysis of the lateral geniculatenucleus of the cat. J Comp Neurol 73, 405–430.

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Acknowledgements

We wish to thank Dr S. W. Kuffler for his helpful advice andcriticism, and Mr R. B. Bosler and Mr P. E. Lockwood for theirtechnical assistance. This work was supported in part by U.S.Public Health Service grants B-22 and B-1931, and in part byU.S. Air Force contract AF 49 (638)–499 (Air Force Office ofScientific Research, Air Research and Development Command).


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