Skip to main content

Emergence of Orientation Selectivity in the Cerebral Cortex, Modeling

  • Reference work entry
  • First Online:
  • 157 Accesses

Definition

Orientation tuning is a characteristic response property of neurons in primary visual cortex. Models of orientation tuning describe the transformation of response selectivity from lateral geniculate relay cells, which are not orientation selective, to neurons in layer 4 of the primary visual cortex. These models aim to constrain and identify the neural circuitry underlying this canonical transformation in the representation of the visual world.

Detailed Description

Introduction

The overarching goal of systems neuroscience is to explain how the sensory inputs we receive are integrated to generate appropriate behaviors. One method of achieving this goal is to study the mechanisms underlying a single computation and build models which may be applied more generally. Computations performed by the cerebral cortex are amenable to this approach due to the relative uniformity of cortical circuitry. Not only does mammalian cerebral cortex contain a common set of neuron cell types with...

This is a preview of subscription content, log in via an institution.

Buying options

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   2,499.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

References

  • Abbott LF, Varela JA, Sen K, Nelson SB (1997) Synaptic depression and cortical gain control. Science 275:220–224

    CAS  PubMed  Google Scholar 

  • Adorján P, Levitt JB, Lund JS, Obermayer K (1999) A model for the intracortical origin of orientation preference and tuning in macaque striate cortex. Vis Neurosci 16:303–318

    PubMed  Google Scholar 

  • Alitto HJ, Usrey WM (2004) Influence of contrast on orientation and temporal frequency tuning in ferret primary visual cortex. J Neurophysiol 91:2797–2808

    PubMed  Google Scholar 

  • Allison JD, Smith KR, Bonds AB (2001) Temporal-frequency tuning of cross-orientation suppression in the cat striate cortex. Vis Neurosci 18:941–948

    CAS  PubMed  Google Scholar 

  • Anderson JS, Carandini M, Ferster D (2000) Orientation tuning of input conductance, excitation, and inhibition in cat primary visual cortex. J Neurophysiol 84:909–926

    CAS  PubMed  Google Scholar 

  • Banitt Y, Martin KAC, Segev I (2007) A biologically realistic model of contrast invariant orientation tuning by thalamocortical synaptic depression. J Neurosci 27:10230–10239

    CAS  PubMed  Google Scholar 

  • Ben-Yishai R, Lev Bar-Or R, Sompolinsky H (1995) Theory of orientation tuning in visual cortex. Proc Natl Acad Sci USA 92:3844–3848

    PubMed Central  CAS  PubMed  Google Scholar 

  • Bishop PO, Coombs JS, Henry GH (1973) Receptive fields of simple cells in the cat striate cortex. J Physiol (Lond) 231:31–60

    CAS  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Boycott BB, Wässle H (1974) The morphological types of ganglion cells of the domestic cat’s retina. J Physiol 240:397–419

    PubMed Central  CAS  PubMed  Google Scholar 

  • Bringuier V, Chavane F, Glaeser L, Frégnac Y (1999) Horizontal propagation of visual activity in the synaptic integration field of area 17 neurons. Science 283:695–699

    CAS  PubMed  Google Scholar 

  • Bullier J, Henry G (1979) Laminar distribution of first-order neurons and afferent terminals in cat striate cortex. J Neurophysiol 42:1271–1281

    CAS  PubMed  Google Scholar 

  • Carandini M, Ferster D (2000) Membrane potential and firing rate in cat primary visual cortex. J Neurosci 20:470–484

    CAS  PubMed  Google Scholar 

  • Carandini M, Heeger DJ, Senn W (2002) A synaptic explanation of suppression in visual cortex. J Neurosci 22:10053–10065

    CAS  PubMed  Google Scholar 

  • Carandini M, Ringach DL (1997) Predictions of a recurrent model of orientation selectivity. Vision Res 37:3061–3071

    CAS  PubMed  Google Scholar 

  • Cardin JA, Palmer LA, Contreras D (2007) Stimulus feature selectivity in excitatory and inhibitory neurons in primary visual cortex. J Neurosci 27:10333–10344

    PubMed Central  CAS  PubMed  Google Scholar 

  • Chung S, Ferster D (1998) Strength and orientation tuning of the thalamic input to simple cells revealed by electrical evoked cortical suppression. Neuron 20:1177–1189

    CAS  PubMed  Google Scholar 

  • Cleland BG, Levick WR (1974) Properties of rarely encountered types of ganglion cells in the cat’s retina and an overall classification. J Physiol 240:457–492

    PubMed Central  CAS  PubMed  Google Scholar 

  • Crook JM, Kisvárday ZF, Eysel UT (1997) GABA-induced inactivation of functionally characterized sites in cat striate cortex: effects on orientation tuning and direction selectivity. Vis Neurosci 14:141–158

    CAS  PubMed  Google Scholar 

  • DeAngelis GC, Robson JG, Ohzawa I, Freeman RD (1992) Organization of suppression in receptive fields of neurons in cat visual cortex. J Neurophysiol 68:144–163

    CAS  PubMed  Google Scholar 

  • Douglas RJ, Kock C, Mahowald M, Martin KAC, Suarez HH (1995) Recurrent excitation in neocortical circuits. Science 269:981–985

    CAS  PubMed  Google Scholar 

  • Ferster D, Lindström S (1983) An intracellular analysis of geniculate-cortical connectivity in area 17 of the cat. J Physiol 342:181–215

    PubMed Central  CAS  PubMed  Google Scholar 

  • Ferster D, Chung S, Wheat H (1996) Orientation selectivity of thalamic input to simple cells of cat visual cortex. Nature 380:249–252

    CAS  PubMed  Google Scholar 

  • Finn IM, Priebe NJ, Ferster D (2007) The emergence of contrast-invariant orientation tuning in simple cells of cat visual cortex. Neuron 54:137–152

    PubMed Central  CAS  PubMed  Google Scholar 

  • Gardner JL, Anzai A, Ohzawa I, Freeman RD (1999) Linear and nonlinear contributions to orientation tuning of simple cells in the cat’s striate cortex. Vis Neurosci 16:1115–1121

    CAS  PubMed  Google Scholar 

  • Geisler WS, Albrecht DG (1992) Cortical neurons: isolation of contrast gain control. Vision Res 32:1409–1410

    CAS  PubMed  Google Scholar 

  • Gilbert C (1977) Laminar differences in receptive field properties of cells in cat primary visual cortex. J Physiol (Lond) 268:391–421

    CAS  Google Scholar 

  • Gilbert C, Wiesel TN (1979) Morphology and intracortical projections of functionally characterized neurones in the cat visual cortex. Nature 280:120–125

    CAS  PubMed  Google Scholar 

  • Goldberg JA, Rokni U, Sompolinsky H (2004) Patterns of ongoing activity and the functional architecture of the primary visual cortex. Neuron 42:489–500

    CAS  PubMed  Google Scholar 

  • Hammond P (1974) Cat retinal ganglion cells: size and shape of receptive field centres. J Physiol 242:99–118

    PubMed Central  CAS  PubMed  Google Scholar 

  • Hata Y, Tsumoto T, Sato H, Hagihara K, Tamura H (1988) Inhibition contributes to orientation selectivity in visual cortex of cat. Nature 335:815–817

    CAS  PubMed  Google Scholar 

  • Heeger D (1992) Normalization of cell responses in cat striate cortex. Vis Neurosci 9:181–197

    CAS  PubMed  Google Scholar 

  • Hirsch JA, Martinez LM (2006) Circuits that build visual cortical receptive fields. Trends Neurosci 29:30–39

    CAS  PubMed  Google Scholar 

  • Hirsch JA, Alonso JM, Reid RC, Martinez LM (1998) Synaptic integration in striate cortical simple cells. J Neurosci 18:9517–9528

    CAS  PubMed  Google Scholar 

  • Hirsch JA, Martinez LM, Pillai C, Alonso JM, Wang Q, Sommer FT (2003) Functionally distinct inhibitory neurons at the first stages of visual processing. Nat Neurosci 6:1300–1308

    CAS  PubMed  Google Scholar 

  • Hodgkin AL, Huxley AF (1952) A quantitative description of membrane current and its application to conduction and excitation in nerve. J Physiol 117:500–544

    PubMed Central  CAS  PubMed  Google Scholar 

  • Hubel D, Wiesel T (1962) Receptive fields, binocular interaction and functional architecture in the cat’s visual cortex. J Physiol (Lond) 160:106–154

    CAS  Google Scholar 

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

    PubMed Central  CAS  PubMed  Google Scholar 

  • Jagadeesh B, Wheat HS, Kontsevich LL, Tyler CW, Ferster D (1997) Direction selectivity of synaptic potentials in simple cells of the cat visual cortex. J Neurophysiol 78:2772–2789

    CAS  PubMed  Google Scholar 

  • Jones JP and Palmer LA (1987) An evaluation of the two-dimensional Gabor filter model of simple cell receptive fields in cat striate cortex. J Neurophysiol 50(6):1233–1258

    Google Scholar 

  • Kuffler SW (1953) Discharge patterns and functional organization of mammalian retina. J Neurophysiol 16:37–68

    CAS  PubMed  Google Scholar 

  • Lauritzen LZ, Miller KD (2003) Different roles for simple-cell and complex-cell inhibition in V1. J Neurosci 23:10201–10213

    CAS  PubMed  Google Scholar 

  • Leventhal AG, Schall JD (1983) Structural basis of orientation sensitivity of cat retinal ganglion cells. J Comp Neurol 220:465–475

    CAS  PubMed  Google Scholar 

  • Levick WR, Thibos LN (1980) Orientation bias of cat retinal ganglion cells. Nature 286:389–390

    CAS  PubMed  Google Scholar 

  • Markram H, Tsodyks M (1996) Redistribution of synaptic efficacy between neocortical pyramidal neurons. Nature 382:807–810

    CAS  PubMed  Google Scholar 

  • Martin K (1988) From single cells to simple circuits in the cerebral cortex. J Exp Physiol 73:637–702

    CAS  Google Scholar 

  • Martinez LM, Wang Q, Reid RC, Pillai C, Alonso JM, Sommer FT, Hirsch JA (2006) Receptive field structure varies with layer in the primary visual cortex. Nat Neurosci 8:372–379

    Google Scholar 

  • McLaughlin D, Shapely R, Shelley M, Wielaard DJ (2000) A neuronal network model of macaque primary visual cortex (V1): orientation selectivity and dynamics in the input layer of 4Ca. Proc Natl Acad Sci USA 97:8087–8092

    PubMed Central  CAS  PubMed  Google Scholar 

  • Mohanty D, Scholl B, Priebe NJ (2012) The accuracy of membrane potential reconstruction based on spiking receptive fields. J Neurophysiol 107:2143–2153

    PubMed Central  PubMed  Google Scholar 

  • Monier C, Chavane F, Baudot P, Graham LJ, Frégnac Y (2003) Orientation and direction selectivity of synaptic inputs in visual cortical neurons: a diversity of combinations produces spike tuning. Neuron 37(4):663–680

    CAS  PubMed  Google Scholar 

  • Morrone MC, Burr DC, Maffei L (1982) Functional implications of cross-orientation inhibition of cortical visual cells. I. Neurophysiological evidence. Proc R Soc Lond B 216:335–354

    CAS  PubMed  Google Scholar 

  • Nowak LG, Sanchez-Vives MV, McCormick DA (2010) Spatial and temporal features of synaptic to discharge receptive field transformation in cat area 17. J Neurophysiol 103:677–697

    PubMed Central  PubMed  Google Scholar 

  • Ohzawa I, Freeman RD (1986) The binocular organization of simple cells in the cat’s visual cortex. J Neurophysiol 56:221–242

    CAS  PubMed  Google Scholar 

  • Pei X, Vidyasagar TR, Volgushev M, Creutzfeldt OD (1994) Receptive analysis and orientation selectivity of postsynaptic potentials of simple cells in cat visual cortex. J Neurosci 14(11): 7130–7140

    CAS  PubMed  Google Scholar 

  • Pettigrew JD, Nikara T, Bishop PO (1968) Binocular interaction on single unity in cat striate cortex: simultaneous stimulation by single moving slit with receptive fields in correspondence. Exp Brain Res 6:391–410

    CAS  PubMed  Google Scholar 

  • Priebe NJ, Ferster D (2005) Direction selectivity of excitation and inhibition in simple cells of the cat primary visual cortex. Neuron 45:133–145

    CAS  PubMed  Google Scholar 

  • Priebe NJ, Ferster D (2008) Inhibition, spike threshold, and stimulus selectivity in primary visual cortex. Neuron 57:482–490

    CAS  PubMed  Google Scholar 

  • Reid RC, Alonso JM (1995) Specificity of monosynaptic connections from thalamus to visual cortex. Nature 378:281–284

    CAS  PubMed  Google Scholar 

  • Ringach DL, Shapely RM, Hawken MJ (2002) Orientation selectivity in macaque V1: diversity and laminar dependence. J Neurosci 22:5639–5651

    CAS  PubMed  Google Scholar 

  • Sclar G, Freeman RD (1982) Orientation selectivity in the cat’s striate cortex is invariant with stimulus contrast. Exp Brain Res 46:457–461

    CAS  PubMed  Google Scholar 

  • Sharma J, Angelucci A, Sur M (2000) Induction of visual orientation modules in auditory cortex. Nature 404:841–847

    CAS  PubMed  Google Scholar 

  • Shou T, Leventhal AG, Thompson KG, Zhou Y (1995) Direction biases of X and Y type retinal ganglion cells in the cat. J Neurophysiol 73:1414–1421

    CAS  PubMed  Google Scholar 

  • 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

    PubMed Central  CAS  PubMed  Google Scholar 

  • Skottun BC, Bradley A, Sclar G, Ohzawa I, Freeman RD (1987) The effects of contrast on visual orientation and spatial frequency discrimination: a comparison of single cells and behavior. J Neurophysiol 57:773–786

    CAS  PubMed  Google Scholar 

  • Somers DC, Nelson SB, Mriganka S (1995) An emergent model of orientation selectivity in cat visual cortical simple cells. J Neurosci 15:5448–5465

    CAS  PubMed  Google Scholar 

  • Sadogopan S, Ferster D (2012) Feedforward origins of response variability underlying contrast invariant orientation tuning in cat visual cortex. Neuron 74:911–923

    Google Scholar 

  • Stanley GB, Jin J, Wang Y, Desbordes G, Wang Q, Black MJ, Alonso JM (2012) Visual orientation and direction selectivity through thalamic synchrony. J Neurosci 32:9073–9088

    PubMed Central  CAS  PubMed  Google Scholar 

  • Stratford KJ, Tarczy-Hornoch K, Martin KAC, Bannister NJ, Jack JJB (1996) Excitatory synaptic inputs to spiny stellate cells in cat visual cortex. Nature 382:258–261

    CAS  PubMed  Google Scholar 

  • Tanaka K (1983) Cross-correlation analysis of geniculostriate neuronal relationships in cats. J Neurophysiol 49:1303–1318

    CAS  PubMed  Google Scholar 

  • Tao L, Cai D, McLaughlin DW, Shelley MJ, Shapely R (2006) Orientation selectivity in visual cortex by fluctuation-controlled criticality. Proc Natl Acad Sci USA 103:12911–12916

    PubMed Central  CAS  PubMed  Google Scholar 

  • Toyama K, Kimura M, Tanaka K (1981) Organization of cat visual cortex as investigated by cross-correlation technique. J Neurophysiol 46:202–214

    CAS  PubMed  Google Scholar 

  • Troyer TW, Krukowski AE, Priebe NJ, Miller KD (1998) Contrast-invariant orientation tuning in cat visual cortex: thalamocortical input tuning and correlation-based intracortical connectivity. J Neurosci 18:5908–5927

    CAS  PubMed  Google Scholar 

  • Vidyasagar TR, Pei X, Volgushev M (1996) Multiple mechanisms underlying the orientation selectivity of visual cortical neurones. Trends Neurosci 19:272–277

    CAS  PubMed  Google Scholar 

  • Volgushev M, Vidyasagar TR, Pei X (1996) A linear model fails to predict orientation selectivity of cells in cat visual cortex. J Physiol 496:597–606

    PubMed Central  CAS  PubMed  Google Scholar 

  • Wang Q, Webber RM, Stanley GB (2010) Thalamic synchrony and adaptive gating of information flow to cortex. Nat Neurosci 13:1534–1541

    PubMed Central  CAS  PubMed  Google Scholar 

  • Wörgötter F, Koch C (1991) A detailed model of the primary visual pathway in the cat: comparison of afferent excitatory and intracortical inhibitory connection schemes for orientation selectivity. J Neurosci 11:1959–1979

    PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Nicholas J. Priebe .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2015 Springer Science+Business Media New York (outside the USA)

About this entry

Cite this entry

Scholl, B., Priebe, N.J. (2015). Emergence of Orientation Selectivity in the Cerebral Cortex, Modeling. In: Jaeger, D., Jung, R. (eds) Encyclopedia of Computational Neuroscience. Springer, New York, NY. https://doi.org/10.1007/978-1-4614-6675-8_576

Download citation

Publish with us

Policies and ethics