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, and
- Lynne Kiorpes
- Address for correspondence: J. Anthony Movshon, Center for Neural Science, New York University, 4 Washington Place #809, New York, NY 10003, ph: 212 998 7880, email: movshon{at}nyu.edu
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Author contributions: L.E.H., J.A.M., and L.K. designed research; L.E.H., C.S., R.D.K., J.K., V.G.-M., and N.J.M. performed research; L.E.H., C.S., R.D.K., J.K., and V.G.-M. contributed unpublished reagents/analytic tools; L.E.H. analyzed data; L.E.H., C.S., N.J.M., J.A.M., and L.K. wrote the paper.
Abstract
In amblyopia, a visual disorder caused by abnormal visual experience during development, the amblyopic eye loses visual sensitivity while the other (fellow) eye 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 6 female monkeys (Macaca nemestrina) made amblyopic by artificial strabismus or anisometropia in early life, as well as 2 visually normal female monkeys (Macaca nemestrina). To measure suppressive binocular interactions directly, we recorded neuronal responses to dichoptic stimulation. We simultaneously stimulated both eyes 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 fellow eye dominated amblyopic visual cortex, especially in more severe amblyopes, but suppression from both the fellow and amblyopic eyes was prevalent in all animals. This imbalance created strong interocular suppression in deep amblyopes: increasing contrast in the amblyopic eye 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 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, while 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.
Footnotes
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The authors declare no competing financial interests.
- Received February 16, 2017.
- Revision received June 21, 2017.
- Accepted July 14, 2017.
- Copyright © 2017 the authors





