Literature DB >> 28743725

Altered Balance of Receptive Field Excitation and Suppression in Visual Cortex of Amblyopic Macaque Monkeys.

Luke E Hallum1, Christopher Shooner2, Romesh D Kumbhani2, Jenna G Kelly2, Virginia García-Marín2, Najib J Majaj2, J Anthony Movshon2, Lynne Kiorpes2.   

Abstract

In amblyopia, a visual disorder caused by abnormal visual experience during development, the amblyopic eye (AE) loses visual sensitivity whereas the fellow eye (FE) is largely unaffected. Binocular vision in amblyopes is often disrupted by interocular suppression. We used 96-electrode arrays to record neurons and neuronal groups in areas V1 and V2 of six female macaque monkeys (Macaca nemestrina) made amblyopic by artificial strabismus or anisometropia in early life, as well as two visually normal female controls. To measure suppressive binocular interactions directly, we recorded neuronal responses to dichoptic stimulation. We stimulated both eyes simultaneously with large sinusoidal gratings, controlling their contrast independently with raised-cosine modulators of different orientations and spatial frequencies. We modeled each eye's receptive field at each cortical site using a difference of Gaussian envelopes and derived estimates of the strength of central excitation and surround suppression. We used these estimates to calculate ocular dominance separately for excitation and suppression. Excitatory drive from the FE dominated amblyopic visual cortex, especially in more severe amblyopes, but suppression from both the FE and AEs was prevalent in all animals. This imbalance created strong interocular suppression in deep amblyopes: increasing contrast in the AE decreased responses at binocular cortical sites. These response patterns reveal mechanisms that likely contribute to the interocular suppression that disrupts vision in amblyopes.SIGNIFICANCE STATEMENT Amblyopia is a developmental visual disorder that alters both monocular vision and binocular interaction. Using microelectrode arrays, we examined binocular interaction in primary visual cortex and V2 of six amblyopic macaque monkeys (Macaca nemestrina) and two visually normal controls. By stimulating the eyes dichoptically, we showed that, in amblyopic cortex, the binocular combination of signals is altered. The excitatory influence of the two eyes is imbalanced to a degree that can be predicted from the severity of amblyopia, whereas suppression from both eyes is prevalent in all animals. This altered balance of excitation and suppression reflects mechanisms that may contribute to the interocular perceptual suppression that disrupts vision in amblyopes.
Copyright © 2017 the authors 0270-6474/17/378216-11$15.00/0.

Entities:  

Keywords:  anisometropia; binocular interaction; development; interocular perceptual suppression; strabismus

Mesh:

Year:  2017        PMID: 28743725      PMCID: PMC5566869          DOI: 10.1523/JNEUROSCI.0449-17.2017

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


  61 in total

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2.  Contrast gain control in the visual cortex: monocular versus binocular mechanisms.

Authors:  A M Truchard; I Ohzawa; R D Freeman
Journal:  J Neurosci       Date:  2000-04-15       Impact factor: 6.167

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Review 4.  Anatomical origins of the classical receptive field and modulatory surround field of single neurons in macaque visual cortical area V1.

Authors:  Alessandra Angelucci; Jonathan B Levitt; Jennifer S Lund
Journal:  Prog Brain Res       Date:  2002       Impact factor: 2.453

Review 5.  Linking assumptions in amblyopia.

Authors:  Dennis M Levi
Journal:  Vis Neurosci       Date:  2013-07-24       Impact factor: 3.241

6.  Orientation-specific relationship between populations of excitatory and inhibitory lateral connections in the visual cortex of the cat.

Authors:  Z F Kisvárday; E Tóth; M Rausch; U T Eysel
Journal:  Cereb Cortex       Date:  1997 Oct-Nov       Impact factor: 5.357

7.  Dichoptic training enables the adult amblyopic brain to learn.

Authors:  Jinrong Li; Benjamin Thompson; Daming Deng; Lily Y L Chan; Minbin Yu; Robert F Hess
Journal:  Curr Biol       Date:  2013-04-22       Impact factor: 10.834

8.  Asymmetric Dichoptic Masking in Visual Cortex of Amblyopic Macaque Monkeys.

Authors:  Christopher Shooner; Luke E Hallum; Romesh D Kumbhani; Virginia García-Marín; Jenna G Kelly; Najib J Majaj; J Anthony Movshon; Lynne Kiorpes
Journal:  J Neurosci       Date:  2017-07-31       Impact factor: 6.167

9.  Contrast sensitivity and vernier acuity in amblyopic monkeys.

Authors:  L Kiorpes; D C Kiper; J A Movshon
Journal:  Vision Res       Date:  1993-11       Impact factor: 1.886

10.  Keeping an eye on the brain: the role of visual experience in monkeys and children.

Authors:  M L Crawford; R S Harwerth; E L Smith; G K von Noorden
Journal:  J Gen Psychol       Date:  1993-01
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  16 in total

1.  Altered functional interactions between neurons in primary visual cortex of macaque monkeys with experimental amblyopia.

Authors:  Katerina Acar; Lynne Kiorpes; J Anthony Movshon; Matthew A Smith
Journal:  J Neurophysiol       Date:  2019-09-25       Impact factor: 2.714

2.  Understanding the development of amblyopia using macaque monkey models.

Authors:  Lynne Kiorpes
Journal:  Proc Natl Acad Sci U S A       Date:  2019-12-23       Impact factor: 11.205

3.  Asymmetric Dichoptic Masking in Visual Cortex of Amblyopic Macaque Monkeys.

Authors:  Christopher Shooner; Luke E Hallum; Romesh D Kumbhani; Virginia García-Marín; Jenna G Kelly; Najib J Majaj; J Anthony Movshon; Lynne Kiorpes
Journal:  J Neurosci       Date:  2017-07-31       Impact factor: 6.167

4.  Endogenous attention improves perception in amblyopic macaques.

Authors:  Amelie Pham; Marisa Carrasco; Lynne Kiorpes
Journal:  J Vis       Date:  2018-03-01       Impact factor: 2.240

5.  Excitatory Contribution to Binocular Interactions in Human Visual Cortex Is Reduced in Strabismic Amblyopia.

Authors:  Chuan Hou 侯川; Terence L Tyson; Ismet J Uner; Spero C Nicholas; Preeti Verghese
Journal:  J Neurosci       Date:  2021-08-25       Impact factor: 6.167

6.  Contrast Normalization Accounts for Binocular Interactions in Human Striate and Extra-striate Visual Cortex.

Authors:  Chuan Hou; Spero C Nicholas; Preeti Verghese
Journal:  J Neurosci       Date:  2020-02-14       Impact factor: 6.167

7.  Rethinking amblyopia 2020.

Authors:  Dennis M Levi
Journal:  Vision Res       Date:  2020-08-28       Impact factor: 1.886

Review 8.  The Importance of the Interaction Between Ocular Motor Function and Vision During Human Infancy.

Authors:  T Rowan Candy
Journal:  Annu Rev Vis Sci       Date:  2019-09-15       Impact factor: 6.422

9.  Interocular Suppression in Primary Visual Cortex in Strabismus.

Authors:  John R Economides; Daniel L Adams; Jonathan C Horton
Journal:  J Neurosci       Date:  2021-05-03       Impact factor: 6.167

10.  Functionally specific optogenetic modulation in primate visual cortex.

Authors:  Mykyta M Chernov; Robert M Friedman; Gang Chen; Gene R Stoner; Anna Wang Roe
Journal:  Proc Natl Acad Sci U S A       Date:  2018-09-26       Impact factor: 11.205

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