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

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 () 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. 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, 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.

Active efficient coding explains the development of binocular vision and its failure in amblyopia

“…This implementation proved sufficient to account for the development of an amblyopia-like state, with mostly monocular receptive fields in the representation of the fovea. More sophisticated suppression models could be incorporated in the future (48,49), but we do not expect them to change the conclusions from the present model. Future work should focus on understanding the principles of interocular suppression within the active efficient coding framework.…”

Active Efficient Coding Explains the Development of Binocular Vision and its Failure in Amblyopia

“…This proved sufficient to account for the development of an amblyopia-like state, with mostly monocular receptive fields in the representation of the fovea. More sophisticated suppression models could be incorporated in the future (42,43), but we do not expect them to change the conclusions from the present model. However, a topic of current interest is how suppression develops during disease and treatment, e.g., with the standard patching method (44).…”

Understanding the development of amblyopia using macaque monkey models

“…4, significant residual interactions persist that are predominantly suppressive (62,63). The appearance of this strong suppression actually results from the reduced excitatory drive from the amblyopic eye, altering the excitatory/inhibitory balance at the local circuit level (74). Moreover, the imbalance of interocular suppression that is evident psychophysically (75)(76)(77)(78)(79), such that the amblyopic eye is more strongly suppressed by the dominant eye than vice versa, is reflected in asymmetric suppression of inputs to binocularly activated neurons in V1 (80).…”