Development of temporal response properties and contrast sensitivity of V1 and V2 neurons in macaque monkeys

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 V

Cortical effects of brief daily periods of unrestricted vision during early monocular form deprivation

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

Effects of perceptual learning on local stereopsis and neuronal responses of V1 and V2 in prism-reared 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 V

Comparisons of interocular suppression in V1 neurons of normal neonatal and infant strabismus monkeys

Background: V1 neurons in neonatal monkeys (6–14 days of age) show a higher prevalence of interocular suppression than in adults to both interocularly matched (iso-oriented) and unmatched (orthogonally-oriented) gratings. However, the prevalence of these suppressive interactions rapidly decreases to normal adult levels by 8 weeks of age (Endo et al, 2001). In this study we investigated how early onset strabismus influenced this normal maturation of binocular signal interactions. Methods: Strabismus was optically simulated in 8 infant rhesus monkeys using a prism-rearing procedure. The onset of strabismus was at 2 weeks of age (before the know onset age for stereopsis), and 4 or 6 weeks of age (after stereopsis onset), and the duration was 14 days (short) and 4 or 8 weeks (long). Immediately after the end of the rearing period, we conducted the microelectrode recording experiments. Results: In all strabismic infants, the binocular signal interactions in V1 neurons were very similar to those that were found in normal neonatal monkeys. Specifically, the strabismic monkeys exhibited a higher than normal prevalence of interocular suppression and the prevalence of interocular suppression for the orthogonally oriented gratings was nearly identical to that for binocularly matched gratings. Conclusions: These findings suggest that the higher than normal prevalence of interocular suppression in V1 in both strabsimic and normal neonatal monkeys has similar underlying causes. One possibility is that the effectiveness of excitatory binocular connections, both local and long-range, is reduced in strabsimic subjects due to early conflicting binocular inputs or in normal neonates due to retinal and/or cortical immaturities, while inhibitory inputs are largely spared or, at least relatively, more mature (Sepigel et al, 1996; Smith et al, 1997; Kumagami et al, 2000)

Time Course of Surround Suppression in V2 Neurons of Macaque Monkeys

In macaque V1, stimulation of the receptive field (RF) surround of a neuron strongly suppresses the responses initiated by stimulation of its classical RF (CRF). Although the exact nature of circuits responsible for surround suppression is still a matter of considerable debate, investigating the time course of surround suppression is a useful means to reveal underlying cortical circuits for suppression (Bair et al, 2003). The previous investigators found that latency of suppression depends on its strength. We previously reported that V2 neurons have similar center/surround organization but exhibit stronger surround suppression than V1 neurons (Zhang et al, 2005). In this study using dynamic center-surround stimuli similar to those developed by Bair et al (2003), we examined the time course of surround suppression in 180 V2 neurons and compared to that in 125 V1 neurons in order to determine whether latency of surround suppression is shorter in V2 than in V1 and also how the timing of center/surround responses are different between V1 and V2. We found that the relative latencies of surround suppression and release in V2 were not significantly different from those in V1, and that suppression latency in V2 was generally longer for those units with weaker surround suppression with some notable exceptions. This relationship between suppression latency and the strength of suppression was stronger in V2 than in V1. Other aspects of the timing of center/surround responses were remarkably similar between V1 and V2. These results suggest that circuits in V2 for surround suppression are likely to be similar to those in V1 except that the functional connections supporting surround suppression in V2 are functionally more robust than those in V1

Comparisons of Neuronal Response Reliability Between V1 and V2 of Infant Monkeys

Purpose: : A recent study suggested that both the firing rate and response reliability of individual cortical neurons influence the fidelity and efficiency of information transmitted by individual V1 neurons, and in infant monkeys, the poor firing rates are compensated by higher response reliability (Rust et al, 2002). In this study, we determined whether similar relationships between firing rates and response reliability exist in V2 and if so, whether response reliability is greater in V2 than in V1 in these infant monkeys. Methods: : Microelectrode recording experiments were conducted in V1 and V2 of 2–, 4–, and 8–week–old monkeys to. Receptive fields of all units were located within 4.0 degrees of the center of the fovea. Drifting sine–wave gratings, optimized for each unit with respect to size, spatial frequency, and drift direction, were presented as visual stimuli on a uniform background with mean luminance of 50cd/m2. Responses were measured for gratings of six different contrasts ranging from 0 to 0.5. At each contrast level, responses were obtained in each trial during a period of 640msec for 30 trials. Mutual information was calculated for all contrast pairs and was plotted against the difference in firing rates of each pair. Information density was derived from the fitted curve. Spike count variance to mean ratio during the 640 msec trial period for each contrast was also computed. Results: : V1 and V2 neurons in the first 8 weeks of age showed lower firing rate, but significantly higher information densities and lower variance–to–mean–ratios than those in adults. While there were no significant differences among V1 neurons among infant age groups, V2 neurons at 2 weeks of age showed significantly lower firing rates, higher information densities and lower variance–to–mean–ratios than those in 4– and 8–week–old infants. Conclusions: : As in V1, the lower firing rates of V2 neurons were compensated by their lower response variability, but this reciprocal relationship was far more exaggerated in V2 at two weeks of age than in V1. These results provide additional evidence to support the hypothesis that the functional maturation of cortical neurons proceeds in a hierarchical order

Receptive-Field Center-Surround Organization of V1 and V2 Neurons in 2- and 4-Week-Old Monkeys Under Barbiturate and Non- Barbiturate Anesthesia

Purpose:: We previously reported that the RF center-surround organization of V2 neurons is immature during early development (Zhang et al, PNAS, 2005). Because the receptive-field properties of V2 neurons in neonates may be differentially influenced by the type of anesthetic/analgesic agents that are used for acute microelectrode experiments, we compared the response properties of V1 and V2 neurons at 2- and 4-weeks of age and at maturity in monkeys that were anesthetized with barbiturate or non-barbiturate agents. Methods:: Seven infant and 6 adult macaque monkeys (Macaca mulatta) were prepared for microelectrode recording experiments. Anesthesia was maintained by continuous infusion of one of the following two anesthetic/analgesic agents: 1) Sodium Pentobarbital (Nembutal, 2 mg/kg/hr), or 2) a mixture of Propofol (4 mg/kg/hr)/Sufentanyl citrate (0.05 µg/kg/hr). Results:: Regardless of which anesthesia was used, the average RF center size of V1 and V2 neurons in 2-week-old infants was about 2-3 times as large as those in adults. The majority of V2 units recorded in 2-week-old infants lacked RF surrounds. Surround suppression in V2 was weaker by a factor of 5-6 in 2-week-old infants and by a factor of about 2 in 4-week-old infants. The average peak-firing rate of V2 neurons was lower in 2-week-old infants by a factor of about 3.0 and by a factor of 2.0 in 4-week-old infants compared to that in adults. The temporal response properties and contrast sensitivity of V1 and V2 neurons in infant monkeys exhibited significant immaturities. Conclusions:: The immature RF center/surround organization and substantial immaturities in other response properties of V1 and V2 neurons found in 2- and 4-week-old infants do not reflect the ‘undesirable effects’ that are unique to barbiturate anesthesia

High prevalence of interocular suppression in macaque V1 after only 3 days of early strabismus

Experiencing interocularly conflicting signals early in life results in a higher than normal prevalence of V1 neurons that exhibit binocular suppression. The increase in binocular suppression occurs presumably because the fine balance between excitatory and inhibitory inputs that exist in normal V1 neurons is lost over time in favor of suppressive influences. How interocular suppression becomes the dominant residual binocular interactions in V1 of strabsimic subjects is not well understood. One of the major hypotheses is that increased suppression reflects changes in the relative density of excitatory vs. inhibitory synaptic boutons in the local and/or long-range intrinsic connections in favor of inhibitory connections. We tested this idea by determining whether exceedingly brief periods (3 days) of early strabismus, which are highly unlikely to induce extensive sprouting or retraction in the local and/or long-range intrinsic connections, lead to a high prevalence of suppression. Our microelectrode experiments in anesthetized and paralyzed infant monkeys demonstrated that after 3 days of optical strabismus beginning at 4 weeks of age, the prevalence and magnitude of interocular suppression in V1 greatly increased while the sensitivity of these units to interocular spatial phase disparity was virtually unaffected. This result was in part due to a higher than normal proportion of disparity-sensitive units that also exhibited interocular suppression. Interestingly, longer durations of strabismus (e.g., weeks or months) did not influence the prevalence of binocular suppression. These results suggest that the cortical mechanisms underlying interocular suppression in strabismic monkeys do not necessarily require wholesale changes in the synaptic structure of the intrinsic connections in V1