Abstract
The orientation biases seen in the responses of cells in the retina and dLGN are dependent on the spatial frequency of the stimulus, being appreciable only at higher spatial frequencies. An inhibitory mechanism that suppresses the responses to low spatial frequencies would leave a striate cell receiving a biased geniculate input with an orientation sensitivity at the higher spatial frequencies. Such an inhibition could in fact come from one or a small group of LGN cells (through cortical interneurones), since their response extends to spatial frequencies much lower than for cortical cells at the same eccentricity. According to this scheme, a number of other striate response characteristics, e.g., their length and spatial frequency response functions, can also be explained.
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References
Aersten A, Gerstein GL (1985) Evaluation of neuronal connectivity: sensitivity of cross-correlation. Brain Res 340:341–354
Albus K, Wolf W (1984) Early post-natal development of neuronal function in the kitten's visual cortex: a laminar analysis. J Physiol 348:153–185
Andersen P, Dingledine R, Gjerstad L, Langmoen IA, Mosfeldt-Laursen A (1980) Two different responses of hippocampal pyramidal cells to application of Gamma-amino butyric acid. J Physiol 305:279–296
Andrews BW, Pollen DA (1979) Relationship between spatial frequency selectivity and receptive field profile of simple cells. J Physiol 287:163–176
Appelle S (1972) Perception and discrimination as a function of stimulus orientation: the “oblique effect” in man and animals. Psych Bull 78:266–278
Batschelet E (1965) Statistical methods for the analysis of problems in animal orientation and certain biological rhythms. The American Institute of Biological Sciences, Washington
Bishop PO, Coombs JS, Henry GH (1971) Responses to visual contours: spatio-temporal aspects of excitation in the receptive fields of simple striate neurones. J Physiol 219:625–657
Blakemore C, Van Sluyters RC (1975) Innate and environmental factors in the development of the kitten's visual cortex. J Physiol 248:899–902
Blasdel GG, Salama G (1986) Voltage-sensitive dyes reveal a modular organization in monkey striate cortex. Nature 321:579–585
Bodis-Wollner IG, Pollen DA, Ronner SF (1976) Responses of complex cells in the visual cortex of the cat as a function of the length of moving slits. Brain Res 116:205–216
Bowery NG, Hill DR, Hudson AL, Dobble A, Middlemuss DN, Shaw F, Turnbull M (1980) (-)Baclofen decreases neurotransmitter release in the mammalian CNS by an action at a novel GABA receptor. Nature 283:92–94
Braitenberg V, Braitenberg C (1979) Geometry of orientation columns in the visual cortex. Biol Cybern 33:179–186
Buisseret P, Imbert M (1976) Visual cortical cells: their development properties in normal and dark-reared kittens. J Physiol 255:511–525
Bullier J, Henry GH (1979) Ordinal position of neurones in cat striate cortex. J Neurophysiol 42:1251–1263
Bullier J, Mustari MJ, Henry GH (1982) Receptive-field transformation between LGN neurones and S-cells of cat striate cortex. J Neurophysiol 47:417–438
Cleland BG, Lee BB, Vidyasagar TR (1983) Responses of neurones in the cat's lateral nucleus to moving bars of different length. J Neurosci 3:108–116
Colonnier M (1964) The tangential organization of the cortex. J Anat 98:327–344
Cooper GF, Robson JG (1968) Successive transformations of spatial information in the visual system. IEEE NPL Conf Proc 42:134–143
Creutzfeldt OD, Ito M (1968) Functional synaptic organization of primary visual cortex neurones in the cat. Exp Brain Res 6:324–352
Creutzfeldt OD, Nothdurft HC (1978) Representation of complex visual stimuli in the brain. Naturwissenschaften 65:307–318
Creutzfeldt OD, Innocenti CM, Brooks D (1974a) Vertical organization in the visual cortex (area 17) of the cat. Exp Brain Res 21:315–336
Creutzfeldt OD, Kuhnt U, Benevento LA (1974b) An intracellular analysis of visual cortical neurones to moving stimuli: responses in a co-operative neuronal network. Exp Brain Res 21:251–274
Creutzfeldt OD, Innocenti CM, Brooks D (1975) Neurophysiological experiments on afferent and intrinsic connections in the visual cortex (area 17). In: Gantini M (ed) Golgi Centennial Symposium: Perspectives in neurobiology. Raven Press, New York, pp 319–337
Creutzfeldt OD, Garey LJ, Kuroda R, Wolff JR (1977) The distribution of degenerating axons after small lesions in the intact and isolated visual cortex of the cat. Exp Brain Res 27:419–440
Daniels JD, Norman JL, Pettigrew JD (1977) Biases for oriented moving bars in lateral geniculate nucleus neurones of normal and stripe-reared cats. Exp Brain Res 29:155–172
Dreher B, Sanderson KJ (1973) Receptive field analysis: response to moving contours by single lateral geniculate neurones in the cat. J Neurophysiol 234:95–118
Eysel UT, Wörgötter F (1986) Specific cortical lesions abolish direction selectivity of visual cortical cells in the cat. Soc Neurosci Abstr 12:583
Fairen A, Valverde F (1980) A type of neurone in the visual cortex of cat. A Golgi and electron microscope study of Chandelier cells. J Comp Neurol 194:761–779
Ferster D (1986) Orientation selectivity of synaptic potentials in neurones of cat primary visual cortex. J Neurosci 6:1284–1301
Ferster D, Lindström S (1983) An intracellular analysis of geniculo-cortical connectivity in area 17 of the cat. J Physiol 342:181–215
Fisken RA, Garey LJ, Powell TPS (1975) The intrinsic, association, and commisural connections of area 17 of the visual cortex. Phil Trans R Soc 272:487–536
Frégnac Y, Imbert M (1978) Early development of visual cortical cells in normal and dark-reared kittens: relationship between orientation selectivity and ocular dominance. J Physiol 278:27–44
Freund TF, Martin KAC, Somogyi P, Whitteridge D (1985) Innervation of cat visual areas 17 and 18 by physiologically identified X- and Y-type thalamic afferents. II. Identification of postsynaptic targets by GABA immunocytochemistry and Golgi impregnation. J Comp Neurol 242:275–291
Friedlander MJ, Lin C-S, Stanford LR, Sherman SM (1981) Morphology of functionally identified neurones in the lateral geniculate nucleus of the cat. J Neurophysiol 46:80–129
Fries W, Albus K, Creutzfeldt OD (1977) Effects of interacting visual patterns on single cell responses in cat's striate cortex. Vision Res 17:1001–1008
Gilbert CD (1977) Laminar differences in receptive field properties of cells in cat primary visual cortex. J Physiol 268:391–421
Gilbert CD, Wiesel TN (1979) Morphology and intracortical projections of functionally identified neurones in cat visual cortex. Nature 280:120–125
Gilbert CD, Wiesel TN (1983) Clustered intrinsic connections in cat visual cortex. J Neurosci 3:1116–1133
Hammond P (1974) Cat retinal ganglion cells: size and shape of receptive field centres. J Physiol 242:99–118
Heggelund P (1981a) Receptive field organization of simple cells in cat striates cortex. Exp Brain Res 42:89–98
Heggelund P (1981b) Receptive field organization of complex cells in cat striate cortex. Exp Brain Res 42:99–107
Hendrickson AE, Hunt SP, Wu J-Y (1981) Immunocytochemical localisation of glutamatic acid decarboxylase in monkey striate cortex. Nature 292:605–607
Henry GH, Bishop PO, Dreher B (1974a) Orientation, axis and direction as stimulus parameters for striate cells. Vision Res 14:767–777
Henry GH, Dreher B, Bishop PO (1974b) Orientation specificity of cells in cat striate cortex. J Neurophysiol 37:1394–1409
Henry GH, Goodwin AW, Bishop PO (1978) Spatial summation of responses in receptive fields of single cells in cat striate cortex. Exp Brain Res 32:245–266
Henry GH, Harvey AR, Lund JS (1979) The afferent connections and laminar distribution of cells in the cat striate cortex. J Comp Neurol 187:725–744
Horton JC, Hubel DH (1981) A regular patchy distribution of cytochrome-oxidase staining in primary visual cortex of the macaque monkey. Nature 292:762–764
Hubel DH, Wiesel TN (1962) Receptive fields, binocular interaction and functional architecture in the cat's visual cortex. J Physiol 160:104–154
Hubel DH, Wiesel TN (1968) Receptive fields and functional architekture of monkey striate cortex. J Physiol 195:215–243
Humphrey AL, Hendrickson AE (1980) Radial zones of high metabolic activity in squirrel monkey striate cortex. Soc Neurosci Abstr. 6:315
Kato H, Bishop PO, Orban GA (1978) Hypercomplex and the simple/complex cell classifications in cat striate cortex. J Neurophysiol 41:1071–1095
Kemp JA (1983) Intracellular recordings from rat visual cortical cells in vitro and the action of GABA. J Physiol 349:13P
Koch C, Poggio T (1985) The synaptic veto mechanism: Does it underlie direction and orientation selectivity in the visual cortex? In: Rose D, Dobson VG (eds) Models of the visual cortex. Wiley, New York, pp 408–419
Kulikowski JJ, Bishop PO (1981) Linear analysis of the responses of simple cells in the cat visual cortex. Exp Brain Res 44:386–400
Kulikowski JJ, Vidyasagar TR (1986) Space and spatial frequency: analysis and representation in the macaque striate cortex. Exp Brain Res 64:5–18
Lee BB, Cleland BG, Creutzfeldt OD (1977) The retinal input to cells in area 17 of the cat's cortex. Exp Brain Res 30:527–538
Lehmkuhle S, Kratz KE, Mangel SC, Sherman SM (1980) Spatial and temporal sensitivity of X- and Y-cells in dorsal lateral geniculate nucleus of the cat. J Neurophysiol 43:520–541
Leventhal AG (1983) Relationship between preferred orientation and receptive field position of neurones in cat striate cortex. J Comp Neurol 220:476–483
Leventhal AG, Hirsch HVB (1977) Effects of early experience upon orientation sensitivity and binocularity of neurones in visual cortex of cats. Proc Natl Acad Sci USA 74:1272–1276
Leventhal AG, Hirsch HVB (1980) Receptive-field properties of different classes of neurones in visual cortex of normal and dark-reared cats. J Neurophysiol 43:1111–1132
Leventhal AG, Schall JD (1983) Structural basis of orientation sensitivity of cat retinal ganglion cells. J Comp Neurol 200:465–475
Leventhal AG, Schall JD, Wallace W (1984) Relationship between preferred orientation and receptive field position of neurones in extrastriate cortex (area 19) in the cat. J Comp Neurol 222:445–451
Levick WR, Cleland BG, Dubin MW (1972) Lateral geniculate neurones of cat: retinal inputs and physiology. Invest Ophthalmol Vis Sci 11:302–311
Levick WR, Thibos LN (1982) Analysis of orientation bias in the cat retina. J Physiol 329:243–261
Livingstone MS, Hubel DH (1984) Anatomy and physiology of a color system in the primate visual cortex. J Neurosci 4:309–356
Maffei L, Fiorentini A (1973) The visual cortex as a spatial frequency analyser. Vision Res 13:1255–1267
von der Malsburg C (1973) Self-organization of orientation sensitive cells in the striate cortex. Kybernetik 14:85–100
Mardia KV (1972) Statistics of directional data. Academic Press, London
Martin KAC (1984) Neuronal circuits in cat striate cortex. In: Jones EG, Peters A (ed) Cerebral cortex, vol 2. Plenum Press, New York London, pp 241–284
Martin KAC, Whitteridge D (1984) The relationship of receptive field properties to the dendritic shape of neurones in the cat striate cortex. J Physiol 356:291–302
Michalski A, Gerstein GL, Czarkowska J, Tarnecki R (1983) Interactions between cat striate cortex neurones. Exp Brain Res 51:97–107
Morrone MC, Burr DC, Maffei L (1982) Functional implications of cross-orientation inhibition of cortical visual cells. I. Neurophysiological evidence. Proc R Soc London B 216:335–354
Movshon JA (1975) The velocity tuning of single units in cat striate cortex. J Physiol 249:445–468
Movshon JA, Thompson ID, Tolhurst DJ (1978a) Spatial summation in the receptive fields of simple cells in the cat's striate cortex. J Physiol 283:53–77
Movshon JA, Thompson ID, Tolhurst DJ (1978b) Spatial and temporal contrast sensitivity in neurones in areas 17 and 18 of the cat's visual cortex. J Physiol 283:101–120
Orban GA (1984) Neuronal operations in the visual cortex. Springer, Berlin Heidelberg New York
Orban GA, Kato H, Bishop PO (1979) End-zone region in receptive fields of hypercomplex and other striate neurones in the cat. J Neurophysiol 42:818–832
Orban GA, Kennedy H (1981) The influence of eccentricity on receptive field types and orientation selectivity in areas 17 and 18 of the cat. Brain Res 208:203–208
Orban GA, Kennedy H, Maes H (1981) Response to movement of neurones in areas 17 and 18 of the cat: velocity sensitivity. J Neurophysiol 45:1059–1073
Payne BR, Berman N (1983) Functional organization of neurones in cat striate cortex: variations in preferred orientation and orientation selectivity with receptive field type, ocular dominance and location in visual-field map. J Neurophysiol 49:1051–1072
Payne BR, Berman N, Murphy EH (1980) Organization of direction preferences in cat visual cortex. Brain Res 211:445–450
Pettigrew JD (1974) The effect of visual experience on the development of stimulus specificity by kitten cortical neurones. J Physiol 237:49–74
Ramoa AS, Shadlen M, Skottun BC, Freeman RD (1986) A comparison of inhibition in orientation and spatial frequency selectivity of cat visual cortex. Nature 321:237–239
Rauschecker JP (1984) Neuronal mechanisms of developmental plasticity in the cat's visual system. Human Neurobiol 3:109–114
Rockland KS, Lund JS, Humphrey AL (1982) Anatomical banding of intrinsic connections in striate cortex of tree shrews (Tupaia glis). J Comp Neurol 209:41–58
Rose D (1977) Responses of single units in cat visual cortex to moving bars of light as a function of bar length. J Physiol 271:1–23
Rose D, Dobson VG (1985) Models of the visual cortex. Wiley, New York
Rovamo J, Virsu V, Laurinen P, Hyvarinen L (1982) Resolution of gratings oriented along and across meridians in peripheral retina. Invest Ophthalmol Vis Sci 23:666–670
Schall JD, Vitek DJ, Leventhal AG (1986) Retinal constraints on orientation specificity in cat visual cortex. J Neurosci 6:823–836
Shou T, Ruan D, Zhou Y (1986) The orientation bias of LGN neurones shows topographic relation to area centralis in the cat retina. Exp Brain Res 64:233–236
Sillito AM (1975) The contribution of inhibitory mechanisms to the receptive field properties of neurones in the striate cortex of the cat. J Physiol 250:305–329
Sillito AM (1977) Inhibitory mechanisms underlying the directional selectivity of simple, complex and hypercomplex cells in the cat's visual cortex. J Physiol 271:699–720
Sillito AM (1979) Inhibitory mechanisms influencing complex cell orientation selectivity and their modification at high resting discharge levels. J Physiol 289:33–53
Sillito AM, Versiani V (1977) The contribution of excitatory and inhibitory inputs to the length preference of hypercomplex cells in layers II and III of the cat's striate cortex. J Physiol 273:775–790
Sillito AM, Kemp JA, Milson JA, Berardi N (1980) A reevaluation of the mechanisms underlying simple cell orientation selectivity. Brain Res 194:517–520
Singer W, Tretter F, Cynader M (1975) Organization of cat striate cortex: a correlation of receptive field properties with afferent and efferent connections. J Neurophysiol 38:1080–1098
Somogyi P (1977) A specific “axo-axonal” interneurone in the visual cortex of the rat. Brain Res 136:345–350
Somogyi P, Cowey A (1981) Combined Golgi and electron microscopic study in the synapses formed by double bouquet cells in the visual cortex of the cat and monkey. J Comp Neurol 195:547–566
Tanaka K (1983) Cross-correlation analysis of geniculostriate neuronal relationships in cats. J Neurophysiol 49:1303–1318
Thibos LN, Levick WR (1985) Orientation bias of brisk-transient y-cells of the cat retina for drifting and alternating gratings. Exp Brain Res 58:1–10
Tigwell DA, Lee BB, Sigüenza JA (1984) A comparison of receptive field structure and response phase for simple cells of cat area 17. Neurosci Lett Suppl 18:S164
Tolhurst DJ, Thompson ID (1981) On the variety of spatial frequency selectivities shown by neurones in area 17 of the cat. Proc R Soc London B 213:183–199
Tolkmitt FJ (1977) A computer simulation model of the afferent part of the visual foveation system. Biol Cybern 25:195–203
Toyama K, Matsunami K, Ohno T, Tokashiki S (1974) An intracellular study of neuronal organization in the visual cortex. Exp Brain Res 21:45–66
Toyama K, Kimura M, Tanaka K (1981a) Cross-correlation analysis of interneuronal connectivity in cat visual cortex. J Neurophysiol 46:191–201
Toyama K, Kimura M, Tanaka K (1981b) Organization of cat visual cortex as investigated by cross-correlation techniques. J Neurophysiol 46:202–214
Tretter F, Cynader M, Singer W (1975) Cat parastriate cortex: a primary or secondary visual area? J Neurophysiol 38:1099–1113
Ts'o DY, Gilbert CD, Wiesel TN (1986) Relationships between horizontal interactions and functional architecture in cat striate cortex as revealed by cross-correlation analysis. J Neurosci 6:1160–1170
Tsumoto T, Eckart W, Creutzfeldt OD (1979) Modification of orientation sensitivity of cat visual cortex neurones by removal of GABA-mediated inhibition. Exp Brain Res 34:351–363
Vidyasagar TR (1984) Contribution of inhibitory mechanisms to the orientation sensitivity of cat dLGN neurones. Exp Brain Res 55:192–195
Vidyasagar TR (1985a) Effect of bicuculline on the length-response functions of cat striate cortical cells. J Physiol 358:15P
Vidyasagar TR (1985b) Geniculate orientation biases as Cartesian coordinates for cortical orientation detectors. In: Rose D, Dobson VG (eds) Models of the visual cortex. Wiley, New York, pp 390–395
Vidyasagar TR, Heide W (1984) Geniculate orientation biases seen with moving sine wave gratings: implications for a model of simple cell afferent connectivity. Exp Brain Res 57:196–200
Vidyasagar TR, Sigüenza JA (1985) Relationship between orientation tuning and spatial frequency in neurones of cat area 17. Exp Brain Res 57:628–631
Vidyasagar TR, Urbas JV (1982) Orientation sensitivity of cat LGN neurones with and without inputs from visual cortical areas 17 and 18. Exp Brain Res 46:157–169
Vidyasagar TR, Müller A, Lee BB (1985) Effect of bicuculline on the responses of cat striate cortical cells to moving sine-wave gratings. Neurosci Lett Suppl 22:S297
Watanabe S, Konishi M, Creutzfeldt OD (1966) Postsynaptic potentials in the cat's visual cortex following electrical stimulation of afferent pathways. Exp Brain Res 1:272–283
Watkins DW, Wilson JR, Sherman SM (1978) Receptive-field properties of neurones in binocular and monocular segments of striate cortex in cats raised with binocular lid suture. J Neurophysiol 41:322–337
Wiesel TN, Hubel DH (1965) Comparison of the effects of unilateral and bilateral eye closure on cortical unit responses in kittens. J Neurophysiol 28:1029–1040
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Vidyasagar, T.R. A model of striate response properties based on geniculate anisotropies. Biol. Cybern. 57, 11–23 (1987). https://doi.org/10.1007/BF00318712
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DOI: https://doi.org/10.1007/BF00318712