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Laminar, columnar and topographic aspects of ocular dominance in the primary visual cortex ofCebus monkeys

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Summary

The representation of the two eyes in striate cortex (V1) ofCebus monkeys was studied by electrophysiological single-unit recordings in normal animals and by morphometric analysis of the pattern of ocular dominance (OD) stripes, as revealed by cytochrome oxidase histochemistry in V1 flat-mounts of enucleated animals. Single-unit recordings revealed that the large majority of V1 neurons respond to the stimulation of either eye but are more strongly activated by one of them. As in other species of monkey, neurons with preference for the stimulation of the same eye are grouped in columns 300–400 µm wide, spanning all cortical layers. Monocular neurons are clustered in layer IVc, specially in its deeper half (IVc-beta), and constitute less than 10% of the population of other layers. Neurons with equal responses to each eye are more commonly found in layer V than elsewhere in V1. In the supragranular layers and in granular layer IVc-alpha neurons strongly dominated by one of the eyes tend to be broadly tuned for orientation, while binocularly balanced neurons tend to be sharply tuned for this parameter. No such correlation was detected in the infragranular layers, and most neurons in layer IVc-beta responded regardless of stimulus orientation. Ocular dominance stripes are present throughout most of V1 as long, parallel or bifurcating bands alternately dominated by the ipsi- or the contralateral eye. They are absent from the cortical representations of the blind spot and the monocular crescent. The domains of each eye occupy nearly equal portions of the surface of binocular V1, except for the representation of the periphery, where the contralateral eye has a larger domain, and a narrow strip along the border of V1 with V2, where either eye may predominate. The orderliness of the pattern of stripes and the relationship between stripe arrangement and the representation of the visual meridians vary with eccentricity and polar angle but follow the same rules in different animals. These results demonstrate that the laminar, columnar and topographic distribution of neurons with different degrees of OD in V1 is qualitatively similar in New- and Old World monkeys of similar sizes and suggest that common ancestry, rather than parallel evolution, may account for the OD phenotypes of contemporaneous simians.

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References

  • Anderson PA, Olavarria J, Van Sluyters RC (1988) The overall pattern of ocular dominance bands in cat visual cortex. J Neurosc 8:2183–2200

    Google Scholar 

  • Baker FH, Grigg P, von Noorden GK (1974) Effects of visual deprivation and strabismus on the response of neurons in the visual cortex of the monkey, including studies on the striate and prestriate cortex in the normal animal. Brain Res 66:185–208

    Article  Google Scholar 

  • Blakemore C, Garey LJ, Vital-Durand F (1978) The physiological effects of monocular deprivation and their reversal in the monkey's visual cortex. J Physiol (Lond) 283:223–262

    Google Scholar 

  • Blasdel GG, Fitzpatrick D (1984) Physiological organization of layer 4 in macaque striate cortex. J Neurosci 4:880–895

    PubMed  Google Scholar 

  • Blasdel GG, Lund JS, Fitzpatrick D (1985) Intrinsic connections of macaque striate cortex: axonal projections of cells outside lamina 4C. J Neurosci 5:3350–3369

    PubMed  Google Scholar 

  • Bullier J, Henry GH (1980) Ordinal position and afferent input of neurons in monkey striate cortex. J Comp Neurol 193:913–935

    Article  PubMed  Google Scholar 

  • Creutzfeldt OD, Weber H, Tanaka M, Lee BB (1987) Neuronal representation of spectral and spatial stimulus aspects in foveal and parafoveal area 17 of the awake monkey. Exp Brain Res 68:541–564

    Article  PubMed  Google Scholar 

  • Diamond IT, Conley M, Itoh K, Fitzpatrick D (1985) Laminar segregation of geniculocortical projections inGalago senegalensis andAotus trivirgatus. J Comp Neurol 242:584–610

    Article  PubMed  Google Scholar 

  • Dow BM (1974) Functional classes of cells and their laminar distribution in monkey visual cortex. J Neurophysiol 37:927–946

    PubMed  Google Scholar 

  • Fiorani Jr M, Gattass R, Rosa MGP, Sousa APB (1989) Visual area MT in theCebus monkey: location, visuotopic organization and variability. J Comp Neurol 287:98–118

    Article  PubMed  Google Scholar 

  • Fitzpatrick D, Lund JS, Blasdel GG (1985) Intrinsic connections of macaque striate cortex: afferent and efferent connections of lamina 4C. J Neurosci 5:3329–3349

    PubMed  Google Scholar 

  • Fleagle JG (1988) Primate adaptation and evolution. Academic Press, San Diego

    Google Scholar 

  • Florence SL, Conley M, Casagrande VA (1986) Ocular dominance columns and retinal projections in New World spider monkeys(Ateles ater). J Comp Neurol 243:234–248

    Article  PubMed  Google Scholar 

  • Gattass R, Gross CG (1981) Visual topography of the striate projection zone in the posterior superior temporal sulcus (MT) of the macaque. J Neurophysiol 46:621–638

    PubMed  Google Scholar 

  • Gattass R, Rosa MGP, Sousa APB, Pinon MCGP, Fiorani Jr. M, Neuenschwander S (1990) Cortical streams of visual information processing in primates. Brazilian J Med Biol Res 23:375–393

    Google Scholar 

  • Gattass R, Sousa APB, Rosa MGP (1987) Visual topography of V1 in theCebus monkey. J Comp Neurol 259:529–548

    Article  PubMed  Google Scholar 

  • Hawken MJ, Parker AJ (1984) Contrast sensitivity and orientation selectivity in lamina IV of the striate cortex of Old World monkeys. Exp Brain Res 54:367–372

    Article  PubMed  Google Scholar 

  • Hawken MJ, Parker AJ, Lund JS (1988) Laminar organization and constrast sensitivity of direction-selective cells in the striate cortex of the Old World monkey. J Neurosci 8:3541–3548

    PubMed  Google Scholar 

  • Hendrickson AE, Wilson JR, Ogren MP (1978) The neuroanatomical organization of pathways between the dorsal lateral geniculate nucleus and the visual cortex in Old Worlds and New World primates. J Comp Neurol 182:123–136

    Article  PubMed  Google Scholar 

  • Hess DT, Edwards MA (1987) Anatomical demonstration of ocular segregation in the retinogeniculocortical pathway of the New World capuchin monkey(Cebus aplla). J Comp Neurol 264:409–420

    Article  PubMed  Google Scholar 

  • Horton JC (1984) Cytochrome oxidase patches: A new cytoarchitectonic feature of monkey visual cortex. Philos Trans R Soc Lond (Biol) 304:199–253

    Google Scholar 

  • Hubel DH, Freeman DG (1977) Projection into the visual field of ocular dominance columns in macaque monkey. Brain Res 122:336–343

    Article  PubMed  Google Scholar 

  • Hubel DH, Wiesel TN (1968) Receptive fields and functional architecture of monkey striate cortex. J Physiol (Lond) 195:215–243

    Google Scholar 

  • Hubel DH, Wiesel TN (1972) Laminar and columnar distribution of geniculo-cortical fibers in the macaque monkey. J Comp Neurol 146:421–450

    Article  PubMed  Google Scholar 

  • Hubel DH, Wiesel TN (1978) Distribution of inputs from the two eyes to striate cortex of squirrel monkeys. Soc Neurosci Abstr 4:632

    Google Scholar 

  • Hubel DH, Wiesel TN, Le Vay S (1977) Plasticity of ocular dominance columns in monkey striate cortex. Philos Trans R Soc Lond (Biol) 278:377–409

    Google Scholar 

  • Kaas JH, Lin CS, Casagrande VA (1976) The relay of ipsilateral and contralateral retinal input from the lateral geniculate nucleus to striate cortex in the owl monkey: a transneuronal transport study. Brain Res 106:371–378

    Article  PubMed  Google Scholar 

  • Kennedy H, Martin KAC, Orban GA, Whitteridge D (1985) Receptive field properties of neurons in visual area 1 and visual area 2 in the baboon. Neuroscience 14:405–415

    Article  Google Scholar 

  • Law MI, Zahs KR, Stryker MP (1988) Organization of primary visual cortex (Area 17) in the ferret. J Comp Neurol 278:157–180

    Article  PubMed  Google Scholar 

  • Le Vay S, Connoly M, Houde J, Van Essen DC (1985) The complete pattern of ocular dominance stripes in the striate cortex and visual field of the macaque monkey. J Neurosci 5:486–501

    PubMed  Google Scholar 

  • Le Vay SD, Hubel DH, Wiesel TN (1975) The pattern of ocular dominance columns in macaque visual cortex revealed by a reduced silver stain. J Comp Neurol 159:559–576

    Article  PubMed  Google Scholar 

  • Livingstone MS, Hubel DH (1984) Anatomy and physiology of a color system in the primate visual cortex. J Neurosci 4:309–356

    PubMed  Google Scholar 

  • Michael CR (1985) Laminar segregation of color cells in the monkey's striate cortex. Vision Res 25:415–423

    Article  PubMed  Google Scholar 

  • Olavarria J, Van Sluyters RC (1985) Unfolding and flattening the cortex of gyrencephalic brains. J Neurosci Meth 15:191–202

    Article  Google Scholar 

  • Poggio GF, Baker FH, Mansfield RJW, Sillito A, Grigg P (1975) Spatial and chromatic properties of neurons subserving foveal and parafoveal vision in rhesus monkey. Brain Res 100:25–59

    Article  PubMed  Google Scholar 

  • Rosa MGP, Gattass R, Fiorani Jr, M, (1988a) Cytochrome oxidase topography in striate cortex of normal and monocularly enucleatedCebus monkeys. Soc Neurosci Abstr 14:1123

    Google Scholar 

  • Rosa MGP, Gattass R, Fiorani Jr M, (1988b) Complete pattern of ocular dominance stripes in V1 of a New World monkey,Cebus apella. Exp Brain Res 72:645–648

    Article  PubMed  Google Scholar 

  • Rosa MGP, Sousa APB, Gattass R (1988c) Representation of the visual field in the second visual area in theCebus monkey. J Comp Neurol 275:326–345

    Article  PubMed  Google Scholar 

  • Rosa MGP, Gattass R, Soares JGM (1991) A quantitative analysis of cytochrome oxidase-rich patches in the primary visual cortex ofCebus monkeys: topographic distribution and effects of late monocular enucleation. Exp Brain Res 84:195–209

    PubMed  Google Scholar 

  • Rowe MH, Benevento LA, Rezak M (1978) Some observations on the patterns of segregate geniculate inputs to the visual cortex in New World primates: an autoradiographic study. Brain Res 159:371–378

    Article  PubMed  Google Scholar 

  • Schiller PH, Finlay BL, Volman SF (1976) Quantitative studies of single-cell properties in monkey striate cortex. II. Orientation specificity and ocular dominance. J Neurophysiol 39:1320–1333

    PubMed  Google Scholar 

  • Silverman MS, Tootell RBH (1987) Modified technique for cytochrome oxidase histochemistry: increased staining intensity and compatibility with the 2-deoxyglucose autoradiography. J Neurosci Meth 19:1–10

    Article  Google Scholar 

  • Sousa APB, Pinon MCGP, Gattass R, Rosa MGP (1991) Topographic organization of cortical input to striate cortex in theCebus monkey: a fluorescent tracer study. J Comp Neurol 308:665–682

    Article  PubMed  Google Scholar 

  • Spatz WB (1979) The retino-geniculo-cortical pathway inCallithrix. II. The geniculo-cortical projection. Exp Brain Res 36:401–410

    Article  PubMed  Google Scholar 

  • Spatz WB (1989) Loss of ocular dominance columns with maturity in the monkey,Callithrix jacchus. Brain Res 488:376–380

    Article  PubMed  Google Scholar 

  • Tootell RBH, Silverman MS (1985) Two methods for flat-mounting cortical tissue. J Neurosci Methods 15:177–190

    Article  PubMed  Google Scholar 

  • Tootell RBH, Hamilton SL, Silverman MS, Switkes E (1988) Functional anatomy of macaque striate cortex. I. Ocular dominance, binocular interactions and baseline conditions. J Neurosci 8:1500–1530

    PubMed  Google Scholar 

  • Trusk TC, Kaboord WS, Wong-Riley MTT (1990) Effects of monocular enucleation, tetrodotoxin and lid suture on cytochrome-oxidase reactivity in supragranular puffs of adult macaque striate cortex. Vis Neurosci 4:185–204

    PubMed  Google Scholar 

  • Vital-Durand F, Blakemore C (1981) Visual cortex of an anthropoid ape. Nature 291:588–590

    Article  PubMed  Google Scholar 

  • Wong-Riley MTT (1979) Changes in the visual system of monocularly sutured or enucleated cats demonstrable with cytochrome oxidase histochemistry. Brain Res 171:11–28

    Article  PubMed  Google Scholar 

  • Zeki SM (1983) The distribution of wavelength and orientation selective cells in different areas of monkey visual cortex. Proc R Soc Lond (Biol) 217:449–470

    Google Scholar 

Download references

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Author notes

  1. M. G. P. Rosa

    Present address: Vision, Touch and Hearing Research Centre, University of Queensland, 4072, St. Lucia, Australia

Authors and Affiliations

  1. Departamento de Neurobiologia, Instituto de Biofisica Carlos Chagas Filho, Universidade Federal do Rio de Janeiro, Cidade Universitária- CCS- Bloco G- Ilha do Fundão, 21941, Rio de Janeiro RJ, Brazil

    M. G. P. Rosa, R. Gattass, M. Fiorani Jr. & J. G. M. Soares

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  1. M. G. P. Rosa
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  2. R. Gattass
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  3. M. Fiorani Jr.
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  4. J. G. M. Soares
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Rosa, M.G.P., Gattass, R., Fiorani, M. et al. Laminar, columnar and topographic aspects of ocular dominance in the primary visual cortex ofCebus monkeys. Exp Brain Res 88, 249–264 (1992). https://doi.org/10.1007/BF02259100

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