Literature DB >> 33203740

A Model for the Origin of Motion Direction Selectivity in Visual Cortex.

Alan W Freeman1.   

Abstract

Motion perception is a vital part of our sensory repertoire in that it contributes to navigation, awareness of moving objects, and communication. Motion sense in carnivores and primates originates with primary visual cortical neurons selective for motion direction. More than 60 years after the discovery of these neurons, there is still no consensus on the mechanism underlying direction selectivity. This paper describes a model of the cat's visual system in which direction selectivity results from the well-documented orientation selectivity of inhibitory neurons: inhomogeneities in the orientation preference map for inhibitory neurons leads to spatially asymmetric inhibition, and thus to direction selectivity. Stimulation of the model with a drifting grating shows that direction selectivity results from the relative timing of excitatory and inhibitory inputs to a neuron. Using a stationary contrast-reversing grating reveals that the inhibitory input is spatially displaced in the preferred direction relative to the excitatory input, and that this asymmetry leads to the timing difference. More generally, the model yields physiologically realistic estimates of the direction selectivity index, and it reproduces the critical finding with contrast-reversing gratings that response phase advances with grating spatial phase. It is concluded that a model based on intracortical inhibition can account well for the known properties of direction selectivity in carnivores and primates.SIGNIFICANCE STATEMENT Motion perception is vital for navigation, communication, and the awareness of moving objects. Motion sense depends on cortical neurons that are selective for motion direction, and this paper describes a model for the physiological mechanism underlying cortical direction selectivity. The essence of the model is that intracortical inhibition of a direction-selective cell is spatially inhomogeneous and therefore depends on whether a stimulus generates inhibition before or after reaching the cell's receptive field: the response is weaker in the former than in the latter case. If the model is correct, it will contribute to the understanding of motion processing in carnivores and primates.
Copyright © 2021 the authors.

Keywords:  direction selectivity; inhibition; mechanism; model; motion; visual cortex

Mesh:

Year:  2020        PMID: 33203740      PMCID: PMC7786212          DOI: 10.1523/JNEUROSCI.1362-20.2020

Source DB:  PubMed          Journal:  J Neurosci        ISSN: 0270-6474            Impact factor:   6.167


  49 in total

1.  Membrane potential and firing rate in cat primary visual cortex.

Authors:  M Carandini; D Ferster
Journal:  J Neurosci       Date:  2000-01-01       Impact factor: 6.167

2.  The spatial pattern of response magnitude and selectivity for orientation and direction in cat visual cortex.

Authors:  Nicholas V Swindale; Amiram Grinvald; Amir Shmuel
Journal:  Cereb Cortex       Date:  2003-03       Impact factor: 5.357

3.  The derivation of direction selectivity in the striate cortex.

Authors:  Matthew R Peterson; Baowang Li; Ralph D Freeman
Journal:  J Neurosci       Date:  2004-04-07       Impact factor: 6.167

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Authors:  B Jagadeesh; H S Wheat; L L Kontsevich; C W Tyler; D Ferster
Journal:  J Neurophysiol       Date:  1997-11       Impact factor: 2.714

5.  Visual response properties of striate cortical neurons projecting to area MT in macaque monkeys.

Authors:  J A Movshon; W T Newsome
Journal:  J Neurosci       Date:  1996-12-01       Impact factor: 6.167

6.  Comparative electrophysiology of pyramidal and sparsely spiny stellate neurons of the neocortex.

Authors:  D A McCormick; B W Connors; J W Lighthall; D A Prince
Journal:  J Neurophysiol       Date:  1985-10       Impact factor: 2.714

7.  Spatiotemporal energy models for the perception of motion.

Authors:  E H Adelson; J R Bergen
Journal:  J Opt Soc Am A       Date:  1985-02       Impact factor: 2.129

8.  Morphology and mosaic of on- and off-beta cells in the cat retina and some functional considerations.

Authors:  H Wässle; B B Boycott; R B Illing
Journal:  Proc R Soc Lond B Biol Sci       Date:  1981-05-22

9.  Stimulus dependence of orientation and direction sensitivity of cat LGNd relay cells without cortical inputs: a comparison with area 17 cells.

Authors:  K G Thompson; A G Leventhal; Y Zhou; D Liu
Journal:  Vis Neurosci       Date:  1994 Sep-Oct       Impact factor: 3.241

10.  A dedicated circuit links direction-selective retinal ganglion cells to the primary visual cortex.

Authors:  Alberto Cruz-Martín; Rana N El-Danaf; Fumitaka Osakada; Balaji Sriram; Onkar S Dhande; Phong L Nguyen; Edward M Callaway; Anirvan Ghosh; Andrew D Huberman
Journal:  Nature       Date:  2014-02-26       Impact factor: 49.962

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  4 in total

1.  A Computational Model of Direction Selectivity in Macaque V1 Cortex Based on Dynamic Differences between On and Off Pathways.

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Journal:  J Neurosci       Date:  2022-03-03       Impact factor: 6.709

2.  Origins of direction selectivity in the primate retina.

Authors:  Yeon Jin Kim; Beth B Peterson; Joanna D Crook; Hannah R Joo; Jiajia Wu; Christian Puller; Farrel R Robinson; Paul D Gamlin; King-Wai Yau; Felix Viana; John B Troy; Robert G Smith; Orin S Packer; Peter B Detwiler; Dennis M Dacey
Journal:  Nat Commun       Date:  2022-05-23       Impact factor: 17.694

3.  A model for the development of binocular congruence in primary visual cortex.

Authors:  Manula A Somaratna; Alan W Freeman
Journal:  Sci Rep       Date:  2022-07-25       Impact factor: 4.996

4.  A theory of direction selectivity for macaque primary visual cortex.

Authors:  Logan Chariker; Robert Shapley; Michael Hawken; Lai-Sang Young
Journal:  Proc Natl Acad Sci U S A       Date:  2021-08-10       Impact factor: 11.205

  4 in total

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