Receptive-Field Subfields of V2 Neurons in Macaque Monkeys Are Adult-Like Near Birth

Abstract

Infant primates can discriminate texture-defined form despite their relatively low visual acuity. The neuronal mechanisms underlying this remarkable visual capacity of infants have not been studied in nonhuman primates. Since many V2 neurons in adult monkeys can extract the local features in complex stimuli that are required for form vision, we used two-dimensional dynamic noise stimuli and local spectral reverse correlation (LSRC) to measure whether the spatial map of receptive-field subfields in individual V2 neurons is sufficiently mature near birth to capture local features. As in adults, most V2 neurons in 4-week-old monkeys showed a relatively high degree of homogeneity in the spatial matrix of facilitatory subfields. However, about 25% of V2 neurons had the subfield map where the neighboring facilitatory subfields substantially differed in their preferred orientations and spatial frequencies. Over 80% of V2 neurons in both infants and adults had ‘tuned’ suppressive profiles in their subfield maps that could alter the tuning properties of facilitatory profiles. The differences in the preferred orientations between facilitatory and suppressive profiles were relatively large but extended over a broad range. Response immaturities in infants were mild; the overall strength of facilitatory subfield responses was lower than that in adults and the optimal correlation delay (‘latency’) was longer in 4-week-old infants. These results suggest that as early as 4 weeks of age, the spatial receptive-field structure of V2 neurons is as complex as in adults and the ability of V2 neurons to compare local features of neighboring stimulus elements is nearly adult like.

Sensitivity of vergence responses of 5- to 10-week-old human infants

“…However, it has been shown that the neural architecture necessary for binocular comparisons is present prenatally (Rakic, 1977) and neonatally (Horton & Hocking, 1996) in monkeys. Additional evidence suggests that some neurons in both V1 (Chino et al, 1997) and V2 (Maruko et al, 2008) in neonatal macaques respond to relative disparity, with sensitivity limited only by the spatial frequency tuning of the cell (Zhang et al, 2013). Thus, the present anatomical and physiological evidence supports disparity processing within the first weeks of life in macaque (thought to be roughly equivalent to the first two months of life in humans [Boothe, Dobson, & Teller, 1985]).…”

“…Neurons responding preferentially to different amounts of disparity have been found in the cortex of newborn macaques (Chino, Smith, Hatta, & Cheng, 1997; Maruko et al, 2008; Zhang et al, 2013). Additionally, it has been proposed that the cortical architecture necessary to support disparity processing is present prenatally in monkeys (Horton & Hocking, 1996; Hubel & Wiesel, 1977; Rakic, 1977).…”

Pyramidal cell development: postnatal spinogenesis, dendritic growth, axon growth, and electrophysiology

“…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).…”

Oblique effect in visual area 2 of macaque monkeys

“…The surgical preparation methods have been described elsewhere (Maruko et al, 2008;Tao et al, 2012;Zhang et al, 2013). Briefly, the animals were initially anesthetized with an intramuscular injection of ketamine hydrochloride (20-30 mg/kg) and acepromazine maleate (0.15-0.2 mg/kg).…”

“…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 et al, 2013;Zhang et al, 2005;Zheng et al, 2007).…”