Origins of feature selectivities and maps in the mammalian primary visual cortex
Authors: Trichur R. Vidyasagar, Ulf T. Eysel
Journal: Trends in Neurosciences (2015)

•Cortical feature preferences arise from seeds of subcortical origin.•The cortical selectivity results from inhibition that sharpens biases of thalamic input.•This process also leads to the creation of cortical orientation columns.•Our scheme also explains the formation of ocular dominance columns and ON/OFF domains. A common feature of the mammalian striate cortex is the arrangement of 'orientation domains' containing neurons preferring similar stimulus orientations. They are arranged as spokes of a pinwheel that converge at singularities known as 'pinwheel centers'. We propose that a cortical network of feedforward and intracortical lateral connections elaborates a full set of optimum orientations from geniculate inputs that show a bias to stimulus orientation and form a set of two or a small number of 'Cartesian' coordinates. Because each geniculate afferent carries signals only from one eye and its receptive field (RF) is either ON or OFF center, the network constructs also ocular dominance columns and a quasi-segregation of ON and OFF responses across the horizontal extent of the striate cortex. A common feature of the mammalian striate cortex is the arrangement of 'orientation domains' containing neurons preferring similar stimulus orientations. They are arranged as spokes of a pinwheel that converge at singularities known as 'pinwheel centers'. We propose that a cortical network of feedforward and intracortical lateral connections elaborates a full set of optimum orientations from geniculate inputs that show a bias to stimulus orientation and form a set of two or a small number of 'Cartesian' coordinates. Because each geniculate afferent carries signals only from one eye and its receptive field (RF) is either ON or OFF center, the network constructs also ocular dominance columns and a quasi-segregation of ON and OFF responses across the horizontal extent of the striate cortex. Over 50 years ago, David Hubel and Torsten Wiesel reported what is arguably the single most important discovery about the processing of sensory information by the mammalian brain [1Hubel D.H. Wiesel T.N. Receptive fields, binocular interaction and functional architecture in the cat's visual cortex.J. Physiol. 1962; 160: 106-154Crossref PubMed Scopus (8580) Google Scholar]. They described the remarkable selectivity for the orientation of a bar or edge stimulus in the responses of single neurons in the primary visual cortex of cats, and later also in macaque monkeys [2Hubel D.H. Wiesel T.N. Receptive fields and functional architecture of monkey striate cortex.J. Physiol. 1968; 195: 215-243Crossref PubMed Scopus (4405) Google Scholar]. Although their model of how a cortical neuron acquires the property of orientation selectivity turned out to be one of the most intensely debated issues in visual neuroscience [3Vidyasagar T.R. et al.Multiple mechanisms underlying the orientation selectivity of visual cortical neurones.Trends. Neurosci. 1996; 19: 272-277Abstract Full Text Full Text PDF PubMed Scopus (121) Google Scholar, 4Sompolinsky H. Shapley R. New perspectives on the mechanisms for orientation selectivity.Curr. Opin. Neurobiol. 1997; 7: 514-522Crossref PubMed Scopus (226) Google Scholar, 5Priebe N.J. Ferster D. Mechanisms of neuronal computation in mammalian visual cortex.Neuron. 2012; 75: 194-208Abstract Full Text Full Text PDF PubMed Scopus (131) Google Scholar], it stimulated a plethora of experiments and made the primary visual cortex one of the most studied parts of the brain. Their scheme assumed an excitatory convergence of inputs to a 'simple' cell in layer 4 of the primary visual (striate) cortex from several neurons in the dorsal lateral geniculate nucleus (LGN). In this model, the individual responses of the LGN cells are insensitive to the orientation of the stimulus, but their RFs (see Glossary) are aligned along a row in visual space (Figure 1A). Hubel and Wiesel also proposed, on the basis of both single cell recordings [1Hubel D.H. Wiesel T.N. Receptive fields, binocular interaction and functional architecture in the cat's visual cortex.J. Physiol. 1962; 160: 106-154Crossref PubMed Scopus (8580) Google Scholar, 2Hubel D.H. Wiesel T.N. Receptive fields and functional architecture of monkey striate cortex.J. Physiol. 1968; 195: 215-243Crossref PubMed Scopus (4405) Google Scholar] and autoradiographic studies [6Hubel D.H. Wiesel T.N. Ferrier lecture. Functional architecture of macaque monkey visual cortex.Proc. R. Soc. Lond. B: Biol. Sci. 1977; 198: 1-59Crossref PubMed Google Scholar], that cells tuned to similar properties are clustered together in 'columnar' systems. They described orientation columns in which cells tend to have the same preferred orientation and ocular dominance columns with cells dominated by inputs from the same eye. Subsequent studies with optical imaging of intrinsic signals [7Bartfeld E. Grinvald A. Relationships between orientation-preference pinwheels, cytochrome oxidase blobs, and ocular-dominance columns in primate striate cortex.Proc. Natl. Acad. Sci. U.S.A. 1991; 89: 11905-11909Crossref Scopus (225) Google Scholar] and two-photon calcium imaging [8Ohki K. et al.Highly ordered arrangement of single neurons in orientation pinwheels.Nature. 2006; 442: 925-928Crossref PubMed Scopus (243) Google Scholar] have confirmed and extended this concept. They demonstrated that orientation domains converge at singularities in a manner that resembles the spokes of a pinwheel. Ocular dominance domains and spatial frequency domains also have been reported to have a specific relationship to these pinwheels [9Hübener M. et al.Spatial relationships among three columnar systems in cat area 17.J. Neurosci. 1997; 17: 9270-9284PubMed Google Scholar]. We propose here a novel model where this functional architecture arises from a cortical network operating on sets of stimulus parameters in the geniculate input, such as preference for stimulus orientation, eye of origin of the signals, and ON or OFF center RF, as it generates the feature selectivities of the individual cells. Although the original Hubel and Wiesel model [1Hubel D.H. Wiesel T.N. Receptive fields, binocular interaction and functional architecture in the cat's visual cortex.J. Physiol. 1962; 160: 106-154Crossref PubMed Scopus (8580) Google Scholar] (Figure 1A) of excitatory convergence has been consistent with results of several studies [10Ferster D. Orientation selectivity of synaptic potentials in neurons of cat primary visual cortex.J. Neurosci. 1986; 6: 1284-1301PubMed Google Scholar, 11Reid R.C. Alonso J.M. Specificity of monosynaptic connections from thalamus to visual cortex.Nature. 1995; 378: 281-284Crossref PubMed Scopus (469) Google Scholar, 12Ferster D. et al.Orientation selectivity of thalamic input to simple cells of cat visual cortex.Nature. 1996; 380: 249-252Crossref PubMed Scopus (417) Google Scholar, 13Chapman B. et al.Relation of cortical cell orientation selectivity to alignment of receptive fields of the geniculocortical afferents that arborize within a single orientation column in ferret visual cortex.J. Neurosci. 1991; 11: 1347-1358PubMed Google Scholar, 14Kara P. et al.The spatial receptive field of thalamic inputs to single cortical simple cells revealed by the interaction of visual and electrical stimulation.Proc. Natl. Acad. Sci. U.S.A. 2002; 99: 16261-16266Crossref PubMed Scopus (56) Google Scholar], it has also been seriously challenged. Alternative schemes have promoted other mechanisms in place of or in addition to excitatory convergence to explain orientation selectivity. These include intracortical cross-orientation inhibition [15Creutzfeldt O.D. et al.An intracellular analysis of visual cortical neurones to moving stimuli: response in a co-operative neuronal network.Exp. Brain Res. 1974; 21: 251-274PubMed Google Scholar, 16Sillito A.M. et al.A re-evaluation of the mechanisms underlying simple cell orientation selectivity.Brain Res. 1980; 194: 517-520Crossref PubMed Scopus (191) Google Scholar, 17Eysel U.T. et al.GABA-induced remote inactivation reveals cross-orientation inhibition in the cat striate cortex.Exp. Brain Res. 1990; 80: 626-630Crossref PubMed Scopus (66) Google Scholar, 18Wörgötter F. Eysel U.T. Topographical aspects of intracortical excitation and inhibition contributing to orientation specificity in area 17 of the cat visual cortex.Eur. J. Neurosci. 1991; 3: 1232-1244Crossref PubMed Scopus (28) Google Scholar, 19Pei X. et al.Receptive field analysis and orientation selectivity of postsynaptic potentials of simple cells in cat visual cortex.J. Neurosci. 1994; 14: 7130-7140PubMed Google Scholar, 20Crook J.M. et al.Evidence for a contribution of lateral inhibition to orientation tuning and direction selectivity in cat visual cortex: reversible inactivation of functionally characterized sites combined with neuroanatomical tracing techniques.Eur. J. Neurosci. 1998; 10: 2056-2075Crossref PubMed Scopus (109) Google Scholar] (Figure 1B), intracortical iso-orientation facilitation [3Vidyasagar T.R. et al.Multiple mechanisms underlying the orientation selectivity of visual cortical neurones.Trends. Neurosci. 1996; 19: 272-277Abstract Full Text Full Text PDF PubMed Scopus (121) Google Scholar, 18Wörgötter F. Eysel U.T. Topographical aspects of intracortical excitation and inhibition contributing to orientation specificity in area 17 of the cat visual cortex.Eur. J. Neurosci. 1991; 3: 1232-1244Crossref PubMed Scopus (28) Google Scholar, 21Douglas R.J. et al.An intracellular analysis of the visual responses of neurones in cat visual cortex.J. Physiol. 1991; 440: 659-696Crossref PubMed Scopus (162) Google Scholar, 22Volgushev M. et al.Excitation and inhibition in cortical orientation selectivity revealed by whole cell recordings in vivo.Vis. Neurosci. 1993; 10: 1151-1155Crossref PubMed Scopus (64) Google Scholar, 23Li Y-T. et al.Linear transformation of thalamocortical input by intracortical excitation.Nat. Neurosci. 2013; 16: 1324-1332Crossref PubMed Scopus (108) Google Scholar, 24Lien A.D. Scanziani M. Tuned thalamic excitation is amplified by visual cortical circuits.Nat. Neurosci. 2013; 16: 1315-1323Crossref PubMed Scopus (208) Google Scholar], mild orientation selectivity already present in LGN responses [3Vidyasagar T.R. et al.Multiple mechanisms underlying the orientation selectivity of visual cortical neurones.Trends. Neurosci. 1996; 19: 272-277Abstract Full Text Full Text PDF PubMed Scopus (121) Google Scholar, 25Vidyasagar T.R. Urbas J.V. Orientation sensitivity of cat LGN neurones with and without inputs from visual cortical areas 17 and 18.Exp. Brain Res. 1982; 46: 157-169Crossref PubMed Scopus (143) Google Scholar, 26Schall J.D. et al.Retinal constraints on orientation specificity in cat visual cortex.J. Comp. Neurol. 1986; 241: 1-11Google Scholar, 27Shou T.D. Leventhal A.G. Organized arrangement of orientation-sensitive relay cells in the cat's dorsal lateral geniculate nucleus.J. Neurosci. 1989; 9: 4287-4302PubMed Google Scholar, 28Vidyasagar T.R. A model of striate response properties based on geniculate anisotropies.Biol. Cybern. 1987; 57: 11-23Crossref PubMed Scopus (26) Google Scholar, 29Kuhlmann L. Vidyasagar T.R. A computational study of how orientation bias in the lateral geniculate nucleus can give rise to orientation selectivity in primary visual cortex.Front. Syst. Neurosci. 2011; 5: 81-98Crossref PubMed Scopus (18) Google Scholar] (Figure 1C), ON and OFF spatially offset excitatory inputs [30Soodak R.E. The retinal ganglion cell mosaic defines orientation columns in striate cortex.Proc. Natl. Acad. Sci. U.S.A. 1987; 84: 3936-3940Crossref PubMed Scopus (42) Google Scholar, 31Paik S.B. Ringach D.L. Retinal origin of orientation maps in visual cortex.Nat. Neurosci. 2011; 14: 919-925Crossref PubMed Scopus (87) Google Scholar] (Figure 1D), or LGN cells with adjacent RFs that provide excitatory and inhibitory inputs [32Heggelund P. Receptive field organization of complex cells in cat striate cortex.Exp. Brain Res. 1981; 42: 90-107PubMed Google Scholar] (Figure 1E). Some have also implicated multiple mechanisms in the generation of orientation selectivity [3Vidyasagar T.R. et al.Multiple mechanisms underlying the orientation selectivity of visual cortical neurones.Trends. Neurosci. 1996; 19: 272-277Abstract Full Text Full Text PDF PubMed Scopus (121) Google Scholar, 18Wörgötter F. Eysel U.T. Topographical aspects of intracortical excitation and inhibition contributing to orientation specificity in area 17 of the cat visual cortex.Eur. J. Neurosci. 1991; 3: 1232-1244Crossref PubMed Scopus (28) Google Scholar, 33Somers D.C. et al.An emergent model of orientation selectivity in cat visual cortical simple cells.J. Neurosci. 1995; 15: 5448-5465PubMed Google Scholar]. Much of the discussion on the basis of orientation selectivity has focused on the role of intracortical networks versus feedforward mechanisms in generating the selectivity. Studies that sought to silence cortical networks to observe the 'raw' geniculate input to simple cells reported that the cortical cell excitatory response is already fairly sharply tuned to orientation and does not depend on specific intracortical inhibition from non-optimum orientations [12Ferster D. et al.Orientation selectivity of thalamic input to simple cells of cat visual cortex.Nature. 1996; 380: 249-252Crossref PubMed Scopus (417) Google Scholar, 14Kara P. et al.The spatial receptive field of thalamic inputs to single cortical simple cells revealed by the interaction of visual and electrical stimulation.Proc. Natl. Acad. Sci. U.S.A. 2002; 99: 16261-16266Crossref PubMed Scopus (56) Google Scholar, 23Li Y-T. et al.Linear transformation of thalamocortical input by intracortical excitation.Nat. Neurosci. 2013; 16: 1324-1332Crossref PubMed Scopus (108) Google Scholar, 24Lien A.D. Scanziani M. Tuned thalamic excitation is amplified by visual cortical circuits.Nat. Neurosci. 2013; 16: 1315-1323Crossref PubMed Scopus (208) Google Scholar]. These experiments were not only fraught with a few unavoidable methodological problems [3Vidyasagar T.R. et al.Multiple mechanisms underlying the orientation selectivity of visual cortical neurones.Trends. Neurosci. 1996; 19: 272-277Abstract Full Text Full Text PDF PubMed Scopus (121) Google Scholar, 34Viswanathan S. et al.Role of feedforward geniculate inputs in the generation of orientation selectivity in the cat's primary visual cortex.J. Physiol. 2011; 589: 2349-2361Crossref PubMed Scopus (12) Google Scholar] but, more importantly, one crucial assumption they made for their paradigm to be a valid test of the model of Hubel and Wiesel is contentious. They assume that any orientation selectivity observed in the feedforward input from the thalamus is through a process of excitatory convergence from LGN cells with circular RFs. Such an assumption ignores a large body of evidence for the presence of mild but significant biases to stimulus orientation seen in the responses of cells in the LGN [25Vidyasagar T.R. Urbas J.V. Orientation sensitivity of cat LGN neurones with and without inputs from visual cortical areas 17 and 18.Exp. Brain Res. 1982; 46: 157-169Crossref PubMed Scopus (143) Google Scholar, 26Schall J.D. et al.Retinal constraints on orientation specificity in cat visual cortex.J. Comp. Neurol. 1986; 241: 1-11Google Scholar, 27Shou T.D. Leventhal A.G. Organized arrangement of orientation-sensitive relay cells in the cat's dorsal lateral geniculate nucleus.J. Neurosci. 1989; 9: 4287-4302PubMed Google Scholar, 35Xu X. et al.Are primate lateral geniculate nucleus (LGN) cells really sensitive to orientation or direction?.Vis. Neurosci. 2002; 19: 97-108PubMed Google Scholar, 36Tan A.Y. et al.Orientation selectivity of synaptic input to neurons in mouse and cat primary visual cortex.J. 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In addition, excitatory convergence along the long axis of the RF is also not essential in models that propose either excitation and inhibition on a simple cell arising from two geniculate inputs with spatially offset RFs [32Heggelund P. Receptive field organization of complex cells in cat striate cortex.Exp. Brain Res. 1981; 42: 90-107PubMed Google Scholar] (Figure 1E) or pooling of inputs from adjacent ON and OFF center units [30Soodak R.E. The retinal ganglion cell mosaic defines orientation columns in striate cortex.Proc. Natl. Acad. Sci. U.S.A. 1987; 84: 3936-3940Crossref PubMed Scopus (42) Google Scholar, 31Paik S.B. Ringach D.L. Retinal origin of orientation maps in visual cortex.Nat. Neurosci. 2011; 14: 919-925Crossref PubMed Scopus (87) Google Scholar] (Figure 1D). What is particularly worth noting in the context of the above studies [12Ferster D. et al.Orientation selectivity of thalamic input to simple cells of cat visual cortex.Nature. 1996; 380: 249-252Crossref PubMed Scopus (417) Google Scholar, 14Kara P. et al.The spatial receptive field of thalamic inputs to single cortical simple cells revealed by the interaction of visual and electrical stimulation.Proc. Natl. Acad. Sci. U.S.A. 2002; 99: 16261-16266Crossref PubMed Scopus (56) Google Scholar, 23Li Y-T. et al.Linear transformation of thalamocortical input by intracortical excitation.Nat. Neurosci. 2013; 16: 1324-1332Crossref PubMed Scopus (108) Google Scholar, 24Lien A.D. Scanziani M. Tuned thalamic excitation is amplified by visual cortical circuits.Nat. Neurosci. 2013; 16: 1315-1323Crossref PubMed Scopus (208) Google Scholar] that sought to suppress intracortical activity is the following: a biased thalamic input from even a single LGN cell, when acted upon by any form of suppression [14Kara P. et al.The spatial receptive field of thalamic inputs to single cortical simple cells revealed by the interaction of visual and electrical stimulation.Proc. Natl. Acad. Sci. U.S.A. 2002; 99: 16261-16266Crossref PubMed Scopus (56) Google Scholar, 23Li Y-T. et al.Linear transformation of thalamocortical input by intracortical excitation.Nat. Neurosci. 2013; 16: 1324-1332Crossref PubMed Scopus (108) Google Scholar, 24Lien A.D. Scanziani M. Tuned thalamic excitation is amplified by visual cortical circuits.Nat. Neurosci. 2013; 16: 1315-1323Crossref PubMed Scopus (208) Google Scholar], or reduction in overall response due to cooling [12Ferster D. et al.Orientation selectivity of thalamic input to simple cells of cat visual cortex.Nature. 1996; 380: 249-252Crossref PubMed Scopus (417) Google Scholar], will lead to a residual excitatory response in the cortical cell that will be sharply tuned to orientation, often referred to as the 'tip of the iceberg' effect. Such a possibility has been directly demonstrated by the marked sharpening of the orientation selectivity of LGN cells when subjected to increased inhibition within the LGN itself [34Viswanathan S. et al.Role of feedforward geniculate inputs in the generation of orientation selectivity in the cat's primary visual cortex.J. Physiol. 2011; 589: 2349-2361Crossref PubMed Scopus (12) Google Scholar]. Furthermore, a recent study has shown a close correspondence between the preferred orientation of single LGN afferents to a cortical orientation column and the preferred orientation of the cells in that column [41Vidyasagar T.R. et al.Subcortical orientation biases explain orientation selectivity of visual cortical cells.Physiol. Rep. 2015; 3: e12374Crossref PubMed Scopus (10) Google Scholar]. Such a result will be expected if LGN biases provide the basis for cortical orientation selectivity, but is not predicted by the classical excitatory convergence model. A recent computational study [29Kuhlmann L. Vidyasagar T.R. A computational study of how orientation bias in the lateral geniculate nucleus can give rise to orientation selectivity in primary visual cortex.Front. Syst. Neurosci. 2011; 5: 81-98Crossref PubMed Scopus (18) Google Scholar] showed that the sharp tuning for orientation and spatial frequency of striate cortical cells can be achieved from an orientation-biased geniculate input based on the well-known pattern of geniculate inputs to a striate simple cell, namely monosynaptic excitation and disynaptic inhibition [42Ferster D. Lindstrom S. An intracellular analysis of geniculo-cortical connectivity in area 17 of the cat.J. Physiol. 1983; 342: 181-215Crossref PubMed Scopus (226) Google Scholar]. Such a scheme [28Vidyasagar T.R. A model of striate response properties based on geniculate anisotropies.Biol. Cybern. 1987; 57: 11-23Crossref PubMed Scopus (26) Google Scholar, 29Kuhlmann L. Vidyasagar T.R. A computational study of how orientation bias in the lateral geniculate nucleus can give rise to orientation selectivity in primary visual cortex.Front. Syst. Neurosci. 2011; 5: 81-98Crossref PubMed Scopus (18) Google Scholar] would also explain the length summation seen in cortical cells, namely the increasing response seen with increasing the length of a bar stimulus, to an extent which is often many times the diameter of single LGN RFs. The finding of such length summation was central to the hypothesis of Hubel and Wiesel [1Hubel D.H. Wiesel T.N. Receptive fields, binocular interaction and functional architecture in the cat's visual cortex.J. Physiol. 1962; 160: 106-154Crossref PubMed Scopus (8580) Google Scholar] as in Figure 1A. However, it is to be noted that LGN cells, when tested with bars of different lengths, exhibit the whole spectrum of 'end-inhibition' – from none to almost 100% [43Cleland B.G. et al.Responses of neurons in the cat's lateral geniculate nucleus to moving bars of different length.J. Neurosci. 1983; 3: 183-200Google Scholar]. This range of surround inhibition – expressed via the excitatory and inhibitory inputs from LGN cells to layer 4 simple cells (as in Figure 1C or 1E) – will translate as the typical range seen in the cortex: namely from extensive length summation to the complete suppression of response to a long bar seen in many cortical 'hypercomplex' cells (a detailed account is given in [28Vidyasagar T.R. A model of striate response properties based on geniculate anisotropies.Biol. Cybern. 1987; 57: 11-23Crossref PubMed Scopus (26) Google Scholar]). The length summation is then due to disinhibition rather than to excitatory convergence, except perhaps in the case of layer 6 cells, which seem to receive extensive horizontal inputs from layer 5 cells with co-oriented and coaxially aligned RFs [44Schwartz C. Bolz J. Functional specificity of a long-range horizontal connection in cat visual cortex: a cross-correlational study.J. Neurosci. 1991; 11: 2995-3007PubMed Google Scholar]. Cross-orientation inhibition within the cortex (as in Figure 1B), a widely observed phenomenon and long claimed to sharpen cortical orientation selectivity [15Creutzfeldt O.D. et al.An intracellular analysis of visual cortical neurones to moving stimuli: response in a co-operative neuronal network.Exp. Brain Res. 1974; 21: 251-274PubMed Google Scholar, 16Sillito A.M. et al.A re-evaluation of the mechanisms underlying simple cell orientation selectivity.Brain Res. 1980; 194: 517-520Crossref PubMed Scopus (191) Google Scholar, 17Eysel U.T. et al.GABA-induced remote inactivation reveals cross-orientation inhibition in the cat striate cortex.Exp. Brain Res. 1990; 80: 626-630Crossref PubMed Scopus (66) Google Scholar, 18Wörgötter F. Eysel U.T. Topographical aspects of intracortical excitation and inhibition contributing to orientation specificity in area 17 of the cat visual cortex.Eur. J. Neurosci. 1991; 3: 1232-1244Crossref PubMed Scopus (28) Google Scholar, 19Pei X. et al.Receptive field analysis and orientation selectivity of postsynaptic potentials of simple cells in cat visual cortex.J. Neurosci. 1994; 14: 7130-7140PubMed Google Scholar, 20Crook J.M. et al.Evidence for a contribution of lateral inhibition to orientation tuning and direction selectivity in cat visual cortex: reversible inactivation of functionally characterized sites combined with neuroanatomical tracing techniques.Eur. J. Neurosci. 1998; 10: 2056-2075Crossref PubMed Scopus (109) Google Scholar], has been included in a recent quantitative study of intracortical excitation as one of the cortical mechanisms that might account for part of the observed orientation selectivity of cortical cells that could not be accounted for by excitatory mechanisms [23Li Y-T. et al.Linear transformation of thalamocortical input by intracortical excitation.Nat. Neurosci. 2013; 16: 1324-1332Crossref PubMed Scopus (108) Google Scholar]. The orientation selectivity in the thalamic input is also possibly further sharpened by facilitatory mechanisms within the cortex, such as voltage-sensitive mechanisms within the dendritic tree and intracortical excitation from cells tuned to similar orientations [3Vidyasagar T.R. et al.Multiple mechanisms underlying the orientation selectivity of visual cortical neurones.Trends. Neurosci. 1996; 19: 272-277Abstract Full Text Full Text PDF PubMed Scopus (121) Google Scholar, 18Wörgötter F. Eysel U.T. Topographical aspects of intracortical excitation and inhibition contributing to orientation specificity in area 17 of the cat visual cortex.Eur. J. Neurosci. 1991; 3: 1232-1244Crossref PubMed Scopus (28) Google Scholar, 21Douglas R.J. et al.An intracellular analysis of the visual responses of neurones in cat visual cortex.J. Physiol. 1991; 440: 659-696Crossref PubMed Scopus (162) Google Scholar, 22Volgushev M. et al.Excitation and inhibition in cortical orientation selectivity revealed by whole cell recordings in vivo.Vis. Neurosci. 1993; 10: 1151-1155Crossref PubMed Scopus (64) Google Scholar, 23Li Y-T. et al.Linear transformation of thalamocortical input by intracortical excitation.Nat. Neurosci. 2013; 16: 1324-1332Crossref PubMed Scopus (108) Google Scholar, 24Lien A.D. Scanziani M. Tuned thalamic excitation is amplified by visual cortical circuits.Nat. Neurosci. 2013; 16: 1315-1323Crossref PubMed Scopus (208) Google Scholar]. It has often been pointed out [4Sompolinsky H. Shapley R. New perspectives on the mechanisms for orientation selectivity.Curr. Opin. Neurobiol. 1997; 7: 514-522Crossref PubMed Scopus (226) Google Scholar] that contrast invariance of orientation tuning (namely, the property of striate cortical cells maintaining the same orientation selectivity in the face of changes in the contrast of the visual stimulus) cannot be explained by the classical model of excitatory convergence. However, a combination of mechanisms have been shown to generate the invariance, including greater variability at low contrasts bringing responses to low contrast stimuli above threshold and thus maintaining the same tuning width as at high contrast [45Finn I.M. The emergence of contrast-invariant orientation tuning in simple cells of cat visual cortex.Neuron. 2007; 54: 137-152Abstract Full Text Full Text PDF PubMed Scopus (177) Google Scholar]. However, LGN cells not only exhibit contrast invariance of orientation tuning but also the same higher variance at low contrast as the underlying mechanism for the invariance [46Viswanathan S. et al.Contrast invariance of orientation tuning in the lateral geniculate nucleus of the feline visual system.Eur. J. Neurosci. 2015; (Published online June 16, 2015)https://doi.org/10.1111/ejn.12991Crossref PubMed Scopus (5) Google Scholar]. Most recently, orientation selectivity has not only been shown to be present in geniculate cells in the mouse, but their tuning was found to be equal to that of cells in the primary visual cortex [36Tan A.Y. et al.Orientation selectivity of synaptic input to neurons in mouse and cat primary visual cortex.J. Neurosci. 2011; 31: 12339-12350Crossref PubMed Scopus (88) Google Scholar]. It is an open question whether this reflects a species idiosyncrasy or it is a call for re-evaluation of classical ideas on orientation selectivity in cats, monkeys, tree shrews, and ferrets, who all show sharp tuning for orientation only in the cortex. We suggest that a revision of the classical model is warranted. For such a basic property of the visual system as orientation selectivity, a common strategy – of sharpening a bias inherent in retinal cells – may be adopted across all mammalian species, instead of ignoring the subcortical biases and evolving a new basis for orientation selectivity at the cortical level. Recent work [47Cruz-Martin A. et al.A dedicated circuit linking direction selective retinal ganglion cells to primary visual cortex.Nature. 2014; 507: 358-361Crossref PubMed Scopus (208) Google Scholar] in the mouse has also shown that one class of retinal cells, which are direction- and orientation-specific, project as a dedicated group via the LGN to a specific cortical compartment of orientation-selective cells in the striate cortex. This further supports the concept of retinal specification of cortical orientation selectivity. However, it is worth noting that although the scheme proposed here does not require Hubel and Wiesel type of convergence, and explains several other characteristics that the classical model does not, a small degree of convergence of the LGN cells that provide the orientation bias to cortical ce