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1 Receptive Fields and Maps in the Visual Cortex: Models of Ocular Receptive Fields and Maps in the Visual Cortex Mo dels of Ocular Dominance and Orientation Columns Kenneth D Miller Published in Mo dels of Neural Networks IIIEDomanyJLvan Hemmen and K Schulten Eds SpringerVerlag NY pp Anearlier and briefer version of this article appeared in The Handbook of Neural Networks MAArbib Ed The MIT Press under the ti tle Models of Ocular Dominance and Orientation Columns Reused by permission ABSTRACT The formation of o cular dominance and orientation columns in the mammalian visual cortex is briey reviewed Correlationbased mo d els for their development are then discussed b eginning with the mo dels of Von der Malsburg For the case of semilinear mo dels mo del b ehavior is well understo o d correlations determine receptive eld structure intracor tical interactions determine pro jective eld structure and the knitting together of the two determines the cortical map This provides a ba sis for simple but powerful mo dels of o cular dominance and orientation column formation o cular dominance columns form through a correlation based comp etition b etween lefteye and righteye inputs while orientation columns can form through a comp etition between ONcenter and OFF center inputs These mo dels accountwell for receptive eld structure but are not completely adequate to account for the details of cortical map struc ture Alternative approaches to map structure including the selforganizing feature map of Kohonen are discussed Finally theories of the computa tional function of correlationbased and selforganizing rules are discussed Depts of Physiology and Otolaryngology WM Keck Center for Integra tive Neuroscience and Sloan Center for Theoretical Neurobiology Universityof California San Francisco CA ii Receptive Fields and Maps in the Visual Cortex Postscript version of this gure not available hence gure is omitted from preprint of pap er FIGURE Schematic of the mature visual system Retinal ganglion cells from the two eyes pro ject to separate layers of the lat eral geniculate nucleus LGN Neurons from these twolayers pro ject to separate patches or strip es within layer of visual cortex V Bino cular regions receiv ing input from b oth eyes are depicted at the b orders b etween the eyesp ecic patches The cortex is depicted in crosssection so that layers are ab oveand layers b elow the LGNrecipientlayer Reprinted bypermissionfrom c by the AAAS INTRODUCTION The brain is a learning machine An animals exp erience shap es the neu ral activity of its brain this activity in turn mo dies the brain so that the animal learns from its exp erience This selforganization the brains reshaping of itself through its own activity reviewed in has long fascinated neuroscientists and mo delers The classic example of activitydep endent neural development is the for mation of o cular dominance columns in the cat or monkey primary visual cortex reviewed in The cerebral cortex is the uniquely mammalian part of the brain It is thought to form the complex asso ciative represen tations that characterize mammalian and human intelligence The primary visual cortex V is the rst cortical area to receive visual information It receives signals from the lateral geniculate nucleus of the thalamus LGN which in turn receives input from the retinae of the twoeyes Fig To describ e o cular dominance columns several terms must b e dened First the receptive eld of a cortical cell refers to the area on the retinae in which appropriate light stimulation evokes a resp onse in the cell and also to the pattern of light stimulation that evokes such a resp onse Second a Kenneth D Miller iii Postscript version of this gure not available hence gure is omitted from preprint of pap er FIGURE Ocular dominance columns from cat V A horizontal cut through the layerofVisshown Terminals serving a single eyeare lab eled white Dark regions at edges are out of plane containing LGN terminals Region shown is x mm Photograph generously supplied byDr Y Hata column is dened as follows V extends many millimeters in eachoftwo horizontal dimensions Receptive eld p ositions vary continuously along these dimensions forming a retinotopic map a continuous map of the visual world In the third vertical dimension the cortex is ab out mm in depth and consists of six layers Receptive eld p ositions do not signicantly vary through this depth Such organization in which cortical prop erties are invariant through the vertical depth of cortex but vary horizontallyis called columnar organization and is a basic feature of cerebral cortex Third ocular dominance must b e dened Cells in the LGN are monoc ular resp onding exclusively to stimulation of a single eye Fig LGN cells pro ject to layer of V where they terminate in alternating strip es or patches of terminals representing a single eye Figs Most or in some sp ecies all layer V cells are mono cular Cells in other layers of V resp ond best to the eye that dominates layer resp onses at that horizontal lo cation Thus V cells can be characterized by their ocular dominance or eye preference The strip es or patches of cortex that are dominated throughout the cortical depth by a single eye are known as ocular dominancecolumns The segregated pattern of termination of the LGN inputs to V arises early in development Initially LGN inputs pro ject to layer of V in an overlapping manner without apparent distinction byeye represented The terminal arb ors of individual LGN inputs extend horizontally in layer iv Receptive Fields and Maps in the Visual Cortex for distances as large as mm for comparison a typical spacing b etween cortical cells is p erhaps m Subsequently b eginning either prenatally or shortly after birth dep ending on the sp ecies the inputs representing each eye b ecome horizontally conned to the alternating approximately mm wide o cular dominance patches This segregation results from an activitydep endent comp etition b etween the geniculate terminals serving the twoeyes see discussion in The signal indicating that dierent terminals represent the same eye app ears to be the correlations in their neural activities These correlations exist due b oth to sp ontaneous activity which is lo cally correlated within each retina and to visuallyinduced activity which correlates the activities of retinotopically nearby neurons within each eyeandtoa lesser extent b etween the eyes The segregation pro cess is comp etitive If one eye is caused to have less activity than the other during a critical p erio d in which the columns are forming the more active eye takes over most of the cortical territory but the eye with reduced activity suers no loss of pro jection strength in retinotopic regions in whichitlacks comp etition from the other eye In summary o cular dominance column formation is a simple system in which correlated patterns of neural activity sculpt the patterns of neural connectivity Orientation columns are another striking feature of visual cortical orga nization Most V cells are orientation selective resp onding selectively to lightdark edges over a narrow range of orientations The preferred orienta tion of cortical cells varies regularly and p erio dically across the horizontal dimension of cortex and is invariantinthevertical dimension The matura tion of orientation selectivity is activitydep endent eg However it has not yet b een p ossible to test whether the initial developmentofori entation selectivity is activitydep endent This is b ecause some orien tation selectivity already exists at the earliest developmental times at which vi sual cortical resp onses can be recorded and it has not b een p ossible to blo ck visual system activity immediately b efore this time Nonetheless it has long b een a p opular notion that the initial development of orientation selectivity like that of o cular dominance may o ccur through a pro cess of activitydep endent synaptic comp etition The inputs from LGN to V serving eacheye are of twotyp es ONcenter and OFFcenter Both kinds of cells have circularly symmetric orientation insensitive receptive elds and resp ond to contrast rather than uniform luminance ONcenter cells resp ond to light against a dark background or to light onset OFFcenter cells resp ond to dark against a lightbackground or to light oset In the cat the orientationselectiveVcellsinlayer are simple cel ls cells with receptive elds consisting of alternating oriented subregions that receive exclusively ONcenter or exclusively OFFcenter input Fig As shall b e discussed one theory for the developmentof orientation selectivityis that like o cular dominance it develops through a comp etition b etween two input p opulations in this case a comp etition Kenneth D Miller v FIGURE Two examples of simple cell receptive elds RFs Regions of the visual eld from which a simple cell receives ONcenter white or OFFcenter dark input are shown Note Ocular dominance columns Fig represent an alternation across cortex in the typ e of input left or righteye received by dierent cortical cells while a simple cell RF this gure represents an alternation across visual space in the typ e of input ON or OFFcenter received bya single cortical cell between the ONcenter and the OFFcenter inputs CORRELATIONBASED MODELS To understand o cular dominance and orientation column formation two pro cesses must b e understo o d the developmentofreceptive eld struc ture under what conditions do receptive elds b ecome mono cular drivable only by a single eye or orientation selective the developmentof periodic cortical maps of
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