Binocular interactions in striate cortical neurons of cats reared with discordant visual inputs

Abstract

The postnatal development of cortical binocularity is known to be adversely affected by early abnormal visual experience. However, little information exists on how the signals from the two eyes are combined in individual cortical neurons of animals reared with early discordant binocular visual experience. Since this is a fundamental issue in understanding visual cortical development, we used extracellular single-unit recording methods to study binocular integration in striate cortical neurons of strabismic cats. Specifically, we measured the sensitivity of individual cells to the relative interocular spatial phase of dichoptically presented drifting sinusoidal gratings (i.e., to binocular retinal image disparity). Clear alterations in ocular dominance were observed in all strabismic subjects. Nevertheless, the majority of cortical neurons exhibited some form of binocular interactions when both eyes were stimulated together. The most prominent aspect of cortical physiology in the strabismic animals was the relatively high prevalence of suppressive binocular interactions. Suppression was most frequently found in kittens reared with 2 weeks of early optical dissociation and among adult cats that received 2 weeks of early optical dissociation and a prolonged recovery period. However, substantial excitatory binocular interactions were also maintained in these animals. With an extended period of interocular misalignment (3 or 8 months), all forms of binocular interactions, excitatory and suppressive, were drastically reduced and a greater number of neurons were truly monocular. Although the reduction in the strength of binocular interactions occurred in all units irrespective of their monocular spatial properties, the effect was more pronounced among those units tuned to higher spatial frequencies and this spatial-frequency-dependent effect was larger in the subjects receiving longer periods of binocular dissociation. The results suggest that the "breakdown" of cortical binocular properties in strabismic subjects is not an all-or-none process, and that suppressive binocular interactions may be closely associated with the abnormal binocular interactions exhibited by strabismic humans. Furthermore, our findings are consistent with the notion that cortical disparity-detecting mechanisms are spatial-frequency dependent and, thus, can be selectively altered depending on an animal's early visual experience.

Binocular integration and disparity selectivity in mouse primary visual cortex

“…Across mouse V1 neurons there was no significant difference in DSI values between simple and complex cells ( Fig. 5; Student's t-test, P Ͻ 0.4), but across cat neurons there was a difference between these classes of cells (simple cell mean ϭ 0.37 Ϯ 0.18, complex cell mean ϭ 0.2 Ϯ 0.14; Student's t-test, P Ͻ 0.005), which has been reported previously (Chino et al 1994). Computing disparity selectivity with only the modulation response component in simple cells and the mean response component in complex cells did not change the difference in DSI between cell classes (simple cell mean ϭ 0.36 Ϯ 0.24, complex cell mean ϭ 0.22 Ϯ 0.17; Student's t-test, P Ͻ 0.005).…”

“…3, E and F). These three subsets of simple cells show that binocularity based on ocular dominance and binocular disparity are not necessarily linked (Chino et al 1994;LeVay and Voigt 1988).…”

“…5A; slope ϭ 0.01 Ϯ 0.07, principal component analysis with bootstrapped standard error) or in the cat ( Fig. 5B; slope ϭ 0.08 Ϯ 0.09, principal component analysis with bootstrapped standard error) (Chino et al 1994;LeVay and Voigt 1988). The failure to observe a relationship between the absolute value of ODI R and DSI might be due to the nonlinear relationship between the inputs a neuron receives and its spiking ouput.…”

Acuity-independent effects of visual deprivation on human visual cortex

“…Importantly, suppression prevents stereopsis, the perception of depth from horizontal disparity. Disparity tuning is strongly dependent on normal excitatory interaction, and excitatory inputs from the nonfixating eye are preferentially lost in strabismus (52)(53)(54).…”

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.…”