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

Abstract

The basic sets of cortical connections are present at birth in the primate visual system. The maintenance and refinement of these innate connections are highly dependent on normal visual experience, and prolonged exposure to binocularly uncorrelated signals early in life severely disrupts the normal development of binocular functions. However, very little is known about how rapidly these changes in the functional organization of primate visual cortex emerge or what are the sequence and the nature of the abnormal neural events that occur immediately after experiencing binocular decorrelation. In this study, we investigated how brief periods of ocular misalignment (strabismus) at the height of the critical period alter the cortical circuits that support binocular vision. After only 3 days of optically imposed strabismus, there was a striking increase in the prevalence of V1 neurons that exhibited binocular suppression, i.e., binocular responses were weaker than monocular responses. However, the sensitivity of these neurons to interocular spatial phase disparity was not significantly altered. These contrasting results suggest that the first significant change in V1 caused by early binocular decorrelation is binocular suppression, and that this suppression originates at a site(s) beyond where binocular signals are initially combined.

Fig. 1.

Binocular signal interactions in V1. (a) Stimulation and recording methods. Binocular experiments were conducted by varying relative interocular spatial phase for iso-oriented pairs of gratings. (b) Interocular spatial phase-tuning function from a normal adult monkey. Peak, peak binocular response amplitude; Mean, mean binocular response amplitude; DOM, the dominant monocular response amplitude; ND, the amplitude for the non-dominant eye; Noise, the cell's maintained firing; BII, the amplitude of the fitted sine wave/the average response amplitude; Peak B/M (db), peak binocular response amplitude/monocular response amplitude.

Fig. 2.

ODI of V1 units in 4- and 8-week-old normal infant monkeys and infant monkeys reared with optical strabismus beginning at 4 weeks of age for 3 days, 1 week, and 2 weeks.

Fig. 3.

Interocular spatial phase-tuning functions of V1 units in infant monkeys reared with 3 days of optically imposed strabismus. Note that the unit in b showed both phase tuning and suppression, which was more frequently encountered in monkeys reared with 3 days of strabismus (see Fig. 4).

Fig. 4.

Scatter plots illustrating the disparity sensitivity (BII) of each unit as a function of its peak B/M for normal 4-(a) and 8-week-old monkeys (e), respectively, and monkeys reared with optical strabismus for 3 days (b), 1 week (c), and 2 weeks (d). Histograms on the left of each graph show the frequency distribution of BII and those on the top show the frequency distribution of peak B/M. Filled triangles indicate medians. Data points outside each graph show units with BII >1.0 (top) or Peak B/M exceeding + 6.0 or –6.0 db (sides). The proportion of the disparity sensitive units (BII >0.3, vertical dotted lines)/binocularly suppressive (B/M <0.0, horizontal lines) are also shown. Scale bars with 20% indicate 20% for the frequency histograms. Labeled filled circles correspond to those units illustrated in Fig. 3 as representative neurons.

Fig. 5.

Effects of experiencing brief strabismus on binocular signal interactions in V1 neurons of infant monkeys. (a)(Upper) Mean (±SE) (circles) and median (triangles) BII values of V1 units for normal and strabismic infant monkeys. (Lower) The proportion of disparity sensitive units for normal (open bars) and strabismic infant monkeys (filled bars). (b)(Upper) Mean (±SE) (circles) and median (traingles) peak binocular/monocular response ratios of V1 units for normal and strabismic infant monkeys. (Lower) The proportion of binocularly suppressive units for normal (open bars) and strabismic infant monkeys (filled bars). * and # indicate statistical significance against 4- and 8-week-old normal infants, respectively.

Fig. 6.

Binocular suppression across cortical layers in strabismic and normal infant monkeys. (Upper) Mean (±SE) (circles) and median (triangles) peak binocular/monocular response ratios of V1 units across cortical layers. (Lower) The proportion of binocularly suppressive units for normal (open bars) and strabismic infant monkeys (filled bars) across cortical layers. * and # indicate statistical significance against 4- and 8-week-old normal infants, respectively.