Smith EL 3rd, Chino YM. Development of temporal response properties and contrast sensitivity of V1 and V2 neurons in macaque monkeys. J Neurophysiol 97: 3905-3916, 2007. First published April 11, 2007 doi:10.1152/jn.01320.2006. The temporal contrast sensitivity of human infants is reduced compared to that of adults. It is not known which neural structures of our visual brain sets limits on the early maturation of temporal vision. In this study we investigated how individual neurons in the primary visual cortex (V1) and visual area 2 (V2) of infant monkeys respond to temporal modulation of spatially optimized grating stimuli and a range of stimulus contrasts. As early as 2 wk of age, V1 and V2 neurons exhibited band-pass temporal frequency tuning. However, the optimal temporal frequency and temporal resolution of V1 neurons were much lower in 2-and 4-wk-old infants than in 8-wk-old infants or adults. V2 neurons of 8-wk-old monkeys had significantly lower optimal temporal frequencies and resolutions than those of adults. Onset latency was longer in V1 at 2 and 4 wk of age and was slower in V2 even at 8 wk of age than in adults. Contrast threshold of V1 and V2 neurons was substantially higher in 2-and 4-wk-old infants but became adultlike by 8 wk of age. For the first 4 wk of life, responses to high-contrast stimuli saturated more readily in V2. The present results suggest that although the early development of temporal vision and contrast sensitivity may largely depend on the functional maturation of precortical structures, it is also likely to be limited by immaturities that are unique to V1 and V2.

Neurons in the adult visual cortex are capable of integrating signals over a large area that surrounds their classic receptive field (RF), and this ability of cortical neurons is thought to be intimately involved in perceptual binding. It is not known, however, at what age these long-range signal interactions emerge. Here, we report that qualitatively adult-like center͞surround interactions are already present in the primary visual cortex as early as postnatal day 14 in macaque monkeys. However, the RF surrounds of visual area 2 (V2) neurons were largely absent until 4 weeks of age and, as late as 8 weeks of age, center͞surround signal interactions in V2 neurons were immature. Our results suggest that the cortical circuits underlying the RF center͞surround of individual neurons mature considerably later in V2 than in the primary visual cortex and give critical evidence for the hypothesis that the functional maturation of the primate visual brain proceeds in a hierarchical manner.monkey ͉ postnatal development ͉ primary visual cortex ͉ long-range signal interaction ͉ cortical circuits

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. interocular suppression ͉ long-range interactions ͉ macaque monkeys ͉ strabismus

Experiencing daily brief periods of unrestricted vision during early monocular form deprivation prevents or reduces the degree of resulting amblyopia. To gain insight into the neural basis for these "protective" effects, we analyzed the monocular and binocular response properties of individual neurons in the primary visual cortex (V1) of macaque monkeys that received intermittent unrestricted vision. Microelectrode-recording experiments revealed significant decreases in the proportion of units that were dominated by the treated eyes, and the magnitude of this ocular dominance imbalance was correlated with the degree of amblyopia. The sensitivity of V1 neurons to interocular spatial phase disparity was significantly reduced in all treated monkeys compared with normal adults. With unrestricted vision, however, there was a small but significant increase in overall disparity sensitivity. Binocular suppression was prevalent in monkeys with constant form deprivation but significantly reduced by the daily periods of unrestricted vision. If neurons exhibited consistent responses to stimulation of the treated eye, monocular response properties obtained by stimulation of the two eyes were similar. These results suggest that the observed protective effects of brief periods of unrestricted vision are closely associated with the ability of V1 neurons to maintain their functional connections from the deprived eye and that interocular suppression in V1 may play an important role in regulating synaptic plasticity of these monkeys.

Visual performance improves with practice (perceptual learning). In this study, we sought to determine whether or not adult monkeys reared with early abnormal visual experience improve their stereoacuity by extensive psychophysical training and testing, and if so, whether alterations of neuronal responses in the primary visual cortex (V1) and/or visual area 2 (V2) are involved in such improvement. Strabismus was optically simulated in five macaque monkeys using a prism-rearing procedure between 4 and 14 wk of age. Around 2 yr of age, three of the prism-reared monkeys ("trained" monkeys) were tested for their spatial contrast sensitivity and stereoacuity. Two other prism-reared monkeys received no training or testing ("untrained" monkeys). Microelectrode experiments were conducted around 4 yr of age. All three prism-reared trained monkeys showed improvement in stereoacuity by a factor of 7 or better. However, final stereothresholds were still approximately 10-20 times worse than those in normal monkeys. In V1, disparity sensitivity was drastically reduced in both the trained and untrained prism-reared monkeys and behavioral training had no obvious effect. In V2, the disparity sensitivity in the trained monkeys was better by a factor of approximately 2.0 compared with that in the untrained monkeys. These data suggest that the observed improvement in stereoacuity of the trained prism-reared monkeys may have resulted from better retention of disparity sensitivity in V2 and/or from "learning" by upstream neurons to more efficiently attend to residual local disparity information in V1 and V2.

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