Residual Binocular Interactions in the Striate Cortex of Monkeys Reared With Abnormal Binocular Vision

Abstract

We investigated the nature of residual binocular interactions in the striate cortex (V1) of monkey models for the two most common causes of visual dysfunction in young children, specifically anisometropia and strabismus. Infant rhesus monkeys were raised wearing either anisometropic spectacle lenses that optically defocused one eye or ophthalmic prisms that optically produced diplopia and binocular confusion. Earlier psychophysical investigations had demonstrated that all subjects exhibited permanent binocular vision deficits and, in some cases, amblyopia. When the monkeys were adults, the responses of individual V1 neurons were studied with the use of microelectrode recording techniques while the animals were anesthetized and paralyzed. The manner in which the signals from the two eyes were combined in individual cells was investigated by dichoptically stimulating both eyes simultaneously with drifting sine wave gratings. In both lens- and prism-reared monkeys, fewer neurons had balanced ocular dominances and greater numbers of neurons were excited by only one eye. However, many neurons that appeared to be monocular exhibited clear binocular interactions during dichoptic stimulation. For the surviving binocular neurons, the maximum binocular response amplitudes were lower than normal; fewer neurons, particularly complex cells, were sensitive to relative interocular spatial phase disparities; and the remaining disparity-sensitive neurons exhibited lower degrees of binocular interaction. In prism-reared monkeys, an unusually high proportion of complex cells exhibited binocular suppression during dichoptic stimulation. Binocular contrast summation experiments showed that for both cooperative and antagonistic binocular interactions, contrast signals from the two eyes were combined by individual neurons in a normal linear fashion in both lens- and prism-reared monkeys. The observed binocular deficits appear to reflect a reduction in functional inputs from one eye and/or spatial imprecision in the monocular receptive fields rather than an aberrant form of binocular interaction. In the prism-reared monkeys, the predominance of suppression suggests that inhibitory connections were, however, less susceptible to diplopia and confusion than excitatory connections. Overall, there were many parallels between V1 physiology in our monkey models and the residual vision of humans with anisometropia or strabismus.

Neural mechanisms of recovery following early visual deprivation

“…These studies of the interocular phase sensitivity of cortical cells documented the nature of the residual binocular connections and the remaining selectivity for disparity (Freeman & Ohzawa 1988;Chino et al 1994;Sengpiel et al 1994;Smith et al 1997;Zhang et al 2005). The existence of these residual binocular interactions, which appear to involve predominantly inhibitory mechanisms , provides a potential neural platform for rehabilitation of functional binocular vision in amblyopia.…”

Noise Provides Some New Signals About the Spatial Vision of Amblyopes

“…Abnormal early visual experience results in dramatic deficits in the properties of neurons in cortical area V1 (Wiesel, 1982;Smith et al, 1997;Kiorpes et al, 1998) and in visual perception (Kiorpes and McKee, 1999). For example, if one eye is turned (strabismus) during early childhood, the resulting amblyopia may lead to a loss in the proportion of cortical neurons influenced by the amblyopic eye and a loss of visual acuity, contrast sensitivity, and position acuity (Hess, 1982;Levi, 1991).…”

“…Although the tuning properties of visual neurons in the amblyopic cortex are considered to be normal (Smith et al, 1997;Kiorpes et al, 1998), for many visual tasks, performance may be limited by the information that the observer uses to solve the task. Perceptual task performance is often modeled as the overlap of a "template" with the stimulus plus sources of internal noise (Dosher and Lu, 1999).…”

Rapid plasticity of binocular connections in developing monkey visual cortex (V1)

“…Consequently, binocularly discordant signals early in life dramatically alter visual cortical functions (1,2). For example, early ocular misalignment (strabismus) that disrupts binocular image matching results in a drastic reduction in the proportion of V1 neurons that can be activated by monocular stimulation of either eye (3)(4)(5)(6). Normal binocular signal interactions in the visual cortex of strabismic monkeys are progressively replaced by aberrant residual interactions dominated by binocular suppression (5,7,8).…”

“…For example, early ocular misalignment (strabismus) that disrupts binocular image matching results in a drastic reduction in the proportion of V1 neurons that can be activated by monocular stimulation of either eye (3)(4)(5)(6). Normal binocular signal interactions in the visual cortex of strabismic monkeys are progressively replaced by aberrant residual interactions dominated by binocular suppression (5,7,8). As a result, behaviorally measured local stereopsis is deficient in these monkeys, and binocular suppression becomes a dominant characteristic of their vision (9).…”