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

Luke E. Hallum, Christopher Shooner, Romesh D. Kumbhani, Jenna G. Kelly, Virginia García-Marín, Najib J. Majaj, J. Anthony Movshon, Lynne Kiorpes

Research output: Contribution to journalArticle

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.

Original languageEnglish (US)
Pages (from-to)8216-8226
Number of pages11
JournalThe Journal of neuroscience : the official journal of the Society for Neuroscience
Volume37
Issue number34
DOIs
StatePublished - Aug 23 2017

Fingerprint

Macaca
Visual Cortex
Haplorhini
Amblyopia
Macaca nemestrina
Vision Disorders
Monocular Vision
Anisometropia
ocular Dominance
Binocular Vision
Strabismus
Microelectrodes
Electrodes
Neurons

Keywords

  • anisometropia
  • binocular interaction
  • development
  • interocular perceptual suppression
  • strabismus

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

Altered Balance of Receptive Field Excitation and Suppression in Visual Cortex of Amblyopic Macaque Monkeys. / Hallum, Luke E.; Shooner, Christopher; Kumbhani, Romesh D.; Kelly, Jenna G.; García-Marín, Virginia; Majaj, Najib J.; Movshon, J. Anthony; Kiorpes, Lynne.

In: The Journal of neuroscience : the official journal of the Society for Neuroscience, Vol. 37, No. 34, 23.08.2017, p. 8216-8226.

Research output: Contribution to journalArticle

Hallum, Luke E. ; Shooner, Christopher ; Kumbhani, Romesh D. ; Kelly, Jenna G. ; García-Marín, Virginia ; Majaj, Najib J. ; Movshon, J. Anthony ; Kiorpes, Lynne. / Altered Balance of Receptive Field Excitation and Suppression in Visual Cortex of Amblyopic Macaque Monkeys. In: The Journal of neuroscience : the official journal of the Society for Neuroscience. 2017 ; Vol. 37, No. 34. pp. 8216-8226.
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