Postnatal development of binocular disparity sensitivity in neurons of the primate visual cortex

Abstract

In macaque monkeys, the age at which neurons in the primary visual cortex (V1) become sensitive to interocular image disparities, a prerequisite for stereopsis, is a matter of conjecture. To resolve this fundamental issue in binocular vision development, we measured the responsiveness of individual V1 neurons in anesthetized and paralyzed infant monkeys as a function of the relative, interocular, spatial phase of dichoptic sine-wave gratings. We found that an adult-like proportion of units were sensitive to interocular image disparity as early as the sixth postnatal day, several weeks before the onset age for stereopsis in monkeys. The ocular dominance distributions of cells in infant monkeys were also indistinguishable from those of adults. Thus, at or only a few days after birth, V1 neurons are capable of combining neural signals from the two eyes as in adults and are sensitive to interocular image disparities. However, the monocular spatial-frequency response properties of these disparity-sensitive units were immature, and their overall responsiveness was far lower than that in adults. During the first 4 postnatal weeks, both the spatial frequency response properties and the peak response amplitude rapidly improved, which resulted in a corresponding increase in the absolute sensitivity of individual units to interocular disparity. The results demonstrate that early binocular vision development in monkeys is not constrained by a paucity of disparity-sensitive V1 neurons but, instead, by the relative immaturity of the spatial response properties and the overall unresponsiveness of existing disparity-sensitive neurons.

Fig. 1.

a, Diagram illustrating the methods used to measure the disparity sensitivity of V1 neurons in infant and adult monkeys. Left, Recording setup. Extracellular single-cell recordings were made with a tungsten microelectrode in the operculum of V1 in anesthetized and paralyzed rhesus monkeys.Right, Visual stimulation methods. A pair of identical sinusoidal gratings (corresponding to the cell’s optimal orientation and spatial frequency) were drifted in the unit’s preferred direction (temporal frequency 3.12 Hz; contrast 30–50%), and the relative interocular spatial phase was systematically varied between 0° and 360° in 22.5° steps. b, An example of an interocular phase-tuning function for a simple cell in an adult monkey. The tuning function was obtained by plotting the fundamental Fourier response amplitude (F1) as a function of the relative interocular spatial phase differences. The phase-tuning function was fit with a single cycle of a sine wave. The binocular interaction index (BII) was calculated by taking the ratio of the amplitude of the fitted sine wave over the average response amplitude. A signal-to-noise ratio (S/N) was determined by dividing the amplitude of the fitted sine wave by the residual mean square error of the fit (Ohzawa and Freeman, 1986a; Smith et al., 1996a). Monocular response levels for the left (L) and right (R) eyes are indicated by the filled triangles. The mean binocular responses is indicated by thedotted line. The cell’s maintained firing rate is shown by the open triangle (Noise). The scale bar shows the angular displacement corresponding to a 90° phase shift for sine wave gratings of the unit’s optimal spatial frequency (6 c/d).

Fig. 2.

Ocular dominance distributions of V1 units in infant and adult monkeys. A neuron’s ocular dominance was determined by traditional qualitative methods (Hubel and Wiesel, 1962) and confirmed by comparing the monocular response amplitudes for optimal stimuli (Chino et al., 1994). Ocular dominance 1represents cells driven exclusively by the contralateral eye;7, cells driven exclusively by the ipsilateral eye;4, cells driven equally by both eyes;2–3, 5–6, binocularly activated units dominated by the contralateral or ipsilateral eyes, respectively.

Fig. 3.

An example of monocular and binocular responses from a simple cell in a 6-d-old monkey. a, Polar plots of orientation response functions for the left (open circles) and right (filled circles) eyes. F1 amplitudes were plotted as a function of the direction of stimulus movements. b, Spatial frequency response functions for the left (open circles) and right (filled circles) eyes. Open triangle indicates the cell’s maintained firing rate. c, Binocular phase-tuning function for the same simple cell. The format and conventions are as in Figure 1c.

Fig. 4.

Binocular phase-tuning functions for five representative simple cells (a–e) and five representative complex cells (f–j) from 1-week-old monkeys. The F1 amplitudes for simple cells and the mean response amplitudes for complex cells were plotted as a function of the relative interocular phase differences. The format and conventions are as in Figure 1c.

Fig. 5.

Development of disparity sensitivity in monkey V1.a, Cumulative proportions of cells at each BII value for simple (left) and complex cells (right) in V1 of infant and adult monkeys. b, Cumulative proportion of cells at each S/N value for simple (left) and complex cells (right). No significant differences were found between any of the infant and adult groups (Kruskal–Wallis test, p > 0.1).

Fig. 6.

Scatterplots illustrating the binocular interaction index as a function of the preferred orientation for individual simple (filled circles) and complex cells (open circles). No systematic differences were found between any of the age groups.

Fig. 7.

Orientation and direction selectivity of V1 neurons in infant and adult monkeys. a, Polar plots of responses as a function of stimulus orientation and drift direction in a representative unit from each age group. Response amplitudes were represented by the distance from the origin, and the angular position represents the direction of the grating’s drift. b, The mean ± SE orientation bandwidth as a function of age. Orientation bandwidth for each unit was calculated from its orientation response function at half-maximal response amplitude. c, The mean ± SE direction selectivity as a function of age. A direction selectivity index was calculated by the formula: DI= P − N/P, whereP is the response amplitude for the cell’s preferred direction of stimulus drift and N represents the response to the opposite direction.

Fig. 8.

Development of spatial frequency tuning of V1 neurons in infant monkeys. a, Spatial frequency response functions for representative units from each age group.b, The mean ± SE optimal spatial frequency as a function of age. The data points connected with a dotted line illustrate the responses of the best performing cells for each age group. c, Mean spatial resolution as a function of age. The data for the best performing cells are connected with thedotted line. d, The mean ± SE spatial frequency bandwidths as a function of age. Bandwidth was calculated by the formula: BW (octave) = log₂f₂/f₁, where f₂ and f₁represent the high and low spatial frequencies, respectively, at which the response dropped to half-maximal amplitude. e, The mean ± SE disparity bandwidth of all disparity-sensitive units (filled circles) and the five best-performing cells (open circles) as a function age. Bandwidth was calculated by the formula: BW (arc min) = 60/optimal spatial frequency (c/d) × 0.5. The formula was based on the fact that in a typical disparity-sensitive unit, a 180° phase shift would change the cell’s response from maximum binocular facilitation to maximum binocular suppression.

Fig. 9.

Responsiveness of V1 units in infant and adult monkeys. a, The mean ± SE peak response amplitude obtained under monocular conditions as a function of age.b, The mean ± SE peak response amplitude obtained for the optimal binocular (circles) and monocular (triangles) stimulus conditions during the binocular phase-tuning experiments.