Development of Temporal Response Properties and Contrast Sensitivity of V1 and V2 Neurons in Macaque Monkeys

University of Houston, College of Optometry, 505 J. Davis Armistead Bldg., Houston, TX 77204-2020, USA.
Journal of Neurophysiology (Impact Factor: 2.89). 07/2007; 97(6):3905-16. DOI: 10.1152/jn.01320.2006
Source: PubMed


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.

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Available from: Bin Zhang, Jul 13, 2015
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    • "Although they report that by 4 weeks of age the spatial receptive field structure in V2 is as complex as in adults (Zhang et al., 2013), but their ability to discriminate fine disparity differences was significantly reduced compared with adults (Maruko et al., 2008). V2 neurons of 8-week-old monkeys had significantly lower optimal temporal frequencies and resolutions than those of adults (Zheng et al., 2007). Neurons in area TE do not develop their adult-like response properties until even later in development (Rodman et al., 1993), consistent with our findings of continued growth and branching from birth. "
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    ABSTRACT: Here we review recent findings related to postnatal spinogenesis, dendritic and axon growth, pruning and electrophysiology of neocortical pyramidal cells in the developing primate brain. Pyramidal cells in sensory, association and executive cortex grow dendrites, spines and axons at different rates, and vary in the degree of pruning. Of particular note is the fact that pyramidal cells in primary visual area (V1) prune more spines than they grow during postnatal development, whereas those in inferotemporal (TEO and TE) and granular prefrontal cortex (gPFC; Brodmann's area 12) grow more than they prune. Moreover, pyramidal cells in TEO, TE and the gPFC continue to grow larger dendritic territories from birth into adulthood, replete with spines, whereas those in V1 become smaller during this time. The developmental profile of intrinsic axons also varies between cortical areas: those in V1, for example, undergo an early proliferation followed by pruning and local consolidation into adulthood, whereas those in area TE tend to establish their territory and consolidate it into adulthood with little pruning. We correlate the anatomical findings with the electrophysiological properties of cells in the different cortical areas, including membrane time constant, depolarizing sag, duration of individual action potentials, and spike-frequency adaptation. All of the electrophysiological variables ramped up before 7 months of age in V1, but continued to ramp up over a protracted period of time in area TE. These data suggest that the anatomical and electrophysiological profiles of pyramidal cells vary among cortical areas at birth, and continue to diverge into adulthood. Moreover, the data reveal that the “use it or lose it” notion of synaptic reinforcement may speak to only part of the story, “use it but you still might lose it” may be just as prevalent in the cerebral cortex.
    Frontiers in Neuroanatomy 08/2014; doi: 10.3389/fnana.2014.00078. DOI:10.3389/fnana.2014.00078 · 3.54 Impact Factor
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    • "In another 10 infants, we recorded from both V1 and V2. These infant ages were chosen based on our previous studies on the normal development of V1 and V2; 4 weeks of age is the youngest age when we could reliably analyze the receptive field properties of V1 and V2 neurons, and 8 weeks of age is the critical point of the postnatal development of neuronal development when neuronal responses become very similar to those in adults (Chino, Smith, Hatta, & Cheng, 1997; Maruko et al., 2008; Zhang, Smith, & Chino, 2008; Zhang et al., 2013; Zhang et al., 2005; Zheng et al., 2007). "
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    ABSTRACT: The neural basis of an oblique effect, a reduced visual sensitivity for obliquely oriented stimuli, has been a matter of considerable debate. We have analyzed the orientation tuning of a relatively large number of neurons in the primary visual cortex (V1) and visual area 2 (V2) of anesthetized and paralyzed macaque monkeys. Neurons in V2 but not V1 of macaque monkeys showed clear oblique effects. This orientation anisotropy in V2 was more robust for those neurons that preferred higher spatial frequencies. We also determined whether V1 and V2 neurons exhibit a similar orientation anisotropy soon after birth. The oblique effect was absent in V1 of 4- and 8-week-old infant monkeys, but their V2 neurons showed a significant oblique effect. This orientation anisotropy in infant V2 was milder than that in adults. The results suggest that the oblique effect emerges in V2 based on the pattern of the connections that are established before birth and enhanced by the prolonged experience-dependent modifications of the neural circuitry in V2.
    Journal of Vision 02/2014; 14(2). DOI:10.1167/14.2.3 · 2.39 Impact Factor
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    • "For example, in MT cells showing larger receptive fields had longer response latencies, and higher C50 values. Conceptually, these observations parallel differences observed between the granular and supragranular layers of V1, or between V1 and V2 [46], [51], [52], [53]. However, our data suggest that these relationships are based on mechanisms that are more specific than simple hierarchical convergence. "
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    ABSTRACT: Analysis of the physiological properties of single neurons in visual cortex has demonstrated that both the extent of their receptive fields and the latency of their responses depend on stimulus contrast. Here, we explore the question of whether there are also systematic relationships between these response properties across different cells in a neuronal population. Single unit recordings were obtained from the middle temporal (MT) and dorsomedial (DM) extrastriate areas of anaesthetized marmoset monkeys. For each cell, spatial integration properties (length and width summation, as well as the presence of end- and side-inhibition within 15° of the receptive field centre) were determined using gratings of optimal direction of motion and spatial and temporal frequencies, at 60% contrast. Following this, contrast sensitivity was assessed using gratings of near-optimal length and width. In both areas, we found a relationship between spatial integration and contrast sensitivity properties: cells that summated over smaller areas of the visual field, and cells that displayed response inhibition at larger stimulus sizes, tended to show higher contrast sensitivity. In a sample of MT neurons, we found that cells showing longer latency responses also tended to summate over larger expanses of visual space in comparison with neurons that had shorter latencies. In addition, longer-latency neurons also tended to show less obvious surround inhibition. Interestingly, all of these effects were stronger and more consistent with respect to the selectivity for stimulus width and strength of side-inhibition than for length selectivity and end-inhibition. The results are partially consistent with a hierarchical model whereby more extensive receptive fields require convergence of information from larger pools of "feedforward" afferent neurons to reach near-optimal responses. They also suggest that a common gain normalization mechanism within MT and DM is involved, the spatial extent of which is more evident along the cell's preferred axis of motion.
    PLoS ONE 06/2013; 8(6):e68276. DOI:10.1371/journal.pone.0068276 · 3.23 Impact Factor
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