A psychophysical measurement and analysis of motion perception in normal and binocularly deprived monkeys

PURPOSE. To measure psychophysically the thresholds for motion detection in the nasal and temporal directions under monocular viewing conditions in monkeys reared under conditions of daily alternating monocular occlusion (AMO). The hypothesis was that motion perception would be asymmetric with more sensitivity for motion in the nasal direction. METHODS. Three monkeys subjected to AMO (AMO monkeys) and three normal monkeys were studied. All were trained with operant conditioning techniques to discriminate coherent from random motion in a random dot display. The percentage of dots in the display that moved either left or right was varied. Thresholds for motion detection of nasally directed and temporally directed stimuli were measured to determine whether the motion perception of AMO monkeys was asymmetric, as predicted. RESULTS. A two-factor analysis of variance revealed a statistically significant difference between treatment groups (normal versus AMO) and directions (nasal versus temporal) and a significant interaction. The interaction was due to a significant difference between nasal and temporal directions for the AMO group, but no significant difference for the normal group. Planned comparisons were performed based on each animal's best eye (eye most sensitive to nasal motion) and worst eye (eye least sensitive to temporal motion). No significant differences were found between the two groups in the best eyes' responses to the nasal direction, but the worst eyes' responses in the temporal direction were significantly poorer in the AMO group. A neural model that can account for these findings is based on a Hebbian teacher located in the nucleus of the optic tract that strengthens connections of a subpopulation of directionally selective cortical neurons. CONCLUSIONS. AMO rearing results in asymmetric motion perception. Thresholds for detecting nasally directed motion are normal, whereas thresholds for detecting temporally directed motion are deficient. These results demonstrate that motionprocessing mechanisms in primates exhibit experience-dependent developmental neural plasticity. The locus of the neural plasticity could be a subpopulation of directionally selective neurons in the striate cortex (V1). (Invest Ophthalmol Vis Sci. 2001;42:2547-2553 V isual experience during the early postnatal period plays an important role in development of those parts of the brain that process visual information. 1,2 At birth, human and monkey infants exhibit smooth-pursuit eye movements with stronger responses in the nasal than the temporal direction and asymmetrical monocular optokinetic nystagmus (MOKN) responses characterized by a reduction in the frequency of beats and in amplitude of slow-phase tracking in the temporal direction. 10,11 Evidence of cortical asymmetry in motion processing comes from measurements of visually evoked potentials to motion (MVEP) elicited by oscillating horizontal stimuli. 12-15 MVEP responses produced by human and monkey infants are dominated by the first harmonic component and show responses that are 180°out of phase in the two eyes during monocular viewing. These results have been interpreted as demonstrating that there is a directional bias in neonates that works in opposite directions in the left and right eyes. The neonatal asymmetrical responses to smooth pursuit, MOKN, and MVEPs become symmetrical by approximately 6 months of age in humans and after a few weeks in monkeys. 27 These findings of prolonged motion asymmetries of various forms in visually deprived animals and in humans with infantile esotropia have led to the hypothesis that binocular visual experience during a sensitive period of postnatal development may be crucial to the normal development of motion processing. Studies in humans suggest that the sensitive period associated with asymmetric motion processing may end very early. For example, children who experienced early visual deprivation within the first 6 months of life (early-onset esotropia) displayed MOKN asymmetry, even when the strabismus was corrected, and some amount of binocular fusion finally develFrom th