Visual pathway for the optokinetic reflex in infant macaque monkeys

Abstract

The horizontal optokinetic nystagmus (hOKN) in primates is immature at birth. To elucidate the early functional state of the visual pathway for hOKN, retinal slip neurons were recorded in the nucleus of the optic tract and dorsal terminal nucleus (NOT-DTN) of 4 anesthetized infant macaques. These neurons were direction selective for ipsiversive stimulus movement shortly after birth [postnatal day 9 (P9)], although at a lower direction selectivity index (DSI). The DSI in the older infants (P12, P14, P60) was not different from adults. A total of 96% of NOT-DTN neurons in P9, P12, and P14 were binocular, however, significantly more often dominated by the contralateral eye than in adults. Already in the youngest animals, NOT-DTN neurons were well tuned to different stimulus velocities; however, tuning was truncated toward lower stimulus velocities when compared with adults. As early as at P12, electrical stimulation in V1 elicited orthodromic responses in the NOT-DTN. However, the incidence of activated neurons was much lower in infants (40-60% of the tested NOT-DTN neurons) than in adults (97%). Orthodromic latencies from V1 were significantly longer in P12-P14 (x = 12.2 ± 8.9 ms) than in adults (x = 3.51 ± 0.81 ms). At the same age, electrical stimulation in motion-sensitive area MT was more efficient in activating NOT-DTN neurons (80% of the tested cells) and yielded shorter latencies than in V1 (x = 7.8 ± 3.02 ms; adult x = 2.99 ± 0.85 ms). The differences in discharge rate between neurons in the NOT-DTN contra- and ipsilateral to the stimulated eye are equivalent to the gain asymmetry between monocularly elicited OKN in temporonasal and nasotemporal direction at the various ages.

Figure 1.

A–C, Polar plots of exemplary NOT-DTN neurons recorded in a 1-week-old (A), a 2-week-old (B), and a 2-month-old (C) infant macaque during optokinetic stimulation. Filled symbols and solid lines indicate the neuronal response during visual stimulation, open symbols and dotted lines indicate the neuron's spontaneous activity. In A, the spontaneous activity was recorded in a separate histogram, whereas in B and C, the histogram was divided in spontaneous activity plus activity during movement in one plus activity during movement in the opposite direction. Thus, for the polar plots the spontaneous activity in the histogram of the appropriate stimulus direction was used. Numbers at the outer circle of the plots represent stimulus direction in degrees, numbers along the cardinal axes indicate neuronal activity in spikes/s.

Figure 2.

A–D, Frequency histograms of direction selectivity indices of retinal slip neurons in 1-week-old (A), 2-week-old (B), 2-month-old (C), and adult macaques (D). Abscissa, Direction selectivity index; ordinate, number of cells. Note that in the 1-week-old animal most neurons display only moderate direction selectivity, whereas in older animals more neurons are highly selective.

Figure 3.

A–D, Frequency histograms of the maximal stimulus driven activity recorded from NOT-DTN neurons in 1-week-old (A), 2-week-old (B), 2-month-old (C), and adult macaques (D). Abscissa, Maximal activity in spikes/s; ordinate, number of cells. Maximal activity is markedly lower in infant than in adult macaques.

Figure 4.

A–D, Frequency histograms of visual latencies measured in retinal slip cells of 1-week-old (A), 2-week-old (B), 2-month-old (C), and adult macaques (D). Abscissa, Visual latency in milliseconds; ordinate, number of cells. Visual latencies are significantly longer in infant than in adult monkeys.

Figure 5.

A–C, Velocity tuning curves of retinal slip neurons of 1- and 2-week-old monkeys (A), of a 2-month-old animal (B), and of adult macaques (C). Abscissa, Stimulus velocity in degrees per second; ordinate, response strength in spikes/s. Filled dots with upward error bars and continuous lines indicate the mean activity and SD during stimulation in the preferred direction. Filled triangles, downward error bars, and broken lines indicate the mean activity and SD during stimulation in the non-preferred direction. Open circles and dashed lines indicate the neuronal modulation, i.e., the difference between activity during stimulation in preferred and non-preferred direction.

Figure 6.

A–D, Ocular dominance distributions of retinal slip cells of 1-week-old (A), 2-week-old (B), 2-month-old (C), and adult macaques (D). Abscissa, Ocular dominance groups 1–5 (for definitions, see Materials and Methods); ordinate, percentage of cells. Even though there are many cells driven by both eyes already in very young animals, binocular input is balanced only in adults.

Figure 7.

A, B, Frequency histograms of latencies measured at NOT-DTN neurons after orthodromic electrical stimulation in area V1 (A) and area MT (B). Black bars represent data from 2-week-old macaques, dark gray bars, data from a 2-month-old infant, and light gray bars data from adult monkeys. Abscissa, Orthodromic latencies in milliseconds; ordinate, number of cells. Both V1 and MT-latencies shorten significantly during development.

Figure 8.

Relationship of OKR-asymmetry measured in behavioral experiments (black bars) and NOT-DTN neuronal activity asymmetry measured in electrophysiological experiments (gray bars). Abscissa, Age of the animals in weeks; ordinate, asymmetry index. There is a close similarity and developmental time course of the two parameters. For further explanations see text.