Transient molecular visualization of ocular dominance columns (ODCs) in normal adult marmosets despite the desegregated termination of the retino-geniculo-cortical pathways

Abstract

The activity-dependent immediate early gene protein Krox-24, expressed in the neocortex at high basal levels, decreases rapidly upon neuronal deactivation (Chaudhuri et al. [1995] Vis. Neurosci. 12:35-50). In infant marmosets, as in most primates, the geniculo-cortical terminations segregate into eye-specific anatomical ocular dominance columns (ODCs), which disappear, however, during adolescence (Spatz [1989] Brain Res. 488:376-380), resulting in balanced inputs from the two eyes (Sengpiel et al. [1996] Vis. Neurosci. 13:145-160). Nevertheless, we found, in adult marmosets, 24 hours after monocular retinal activity blockade by tetrodotoxin, distinct alternating compartments of potentiated and depressed Krox-24-like immunoreactivity (Krox-IR) in layer IV of area 17. This pattern of Krox-IR disappeared at 10 days of retinal silencing, but was still present at this survival time in stains for cytochrome oxidase or NADPH-diaphorase. After 20 days of retinal silencing, the pattern was not demonstrable with any of the three stains. We term these compartments physiological ODCs, in contrast to the anatomical ODCs of most primates. If the anatomical ODCs of infant marmosets disappear by collateral sprouting into the inappropriate ODCs, then the collateral geniculo-cortical synapses might differ slightly in their properties from the original ones. We silenced the sets of original and collateral synapses of the one ocularity. This apparently transiently initiated, at the synapses driven by the intact eye, two different complex processes leading to molecular potentiation at the original synapses and to molecular depression at the collateral synapses.

Monocular inhibition reveals temporal and spatial changes in gene expression in the primary visual cortex of marmoset

“…Consistent with the previous report (Markstahler et al, 1998), the active-eye columns were visualized by ISH for ZIF268 in the marmoset visual cortex (Figure 2A). Similar stripe patterns were observed for two other IEGs, ARC and c-FOS , as well (Figures 2B,C).…”

“…A previous study showed the narrow (thin) pale-staining rim below the strong ZIF268 signals in layer IVC in marmoset V1 (Markstahler et al, 1998). From its position, this sublayer is considered as equivalent to the blank sublayer of ZIF268 mRNA observed at 140 min after light induction (showed by the filled star in Figure 5D).…”

“…Among these genes, immediate early genes (IEGs) including c-Fos and Zif268 are defined as the genes that are rapidly and transiently expressed within minutes to several hours from stimulus onset (Morgan et al, 1987; Sheng and Greenberg, 1990), and have been used as the markers for neural activities after sensory stimulation. Studies for how visual stimulation causes the induction of IEGs in the visual cortex have been also done in various mammalian species (Worley et al, 1991; Rosen et al, 1992; Chaudhuri and Cynader, 1993; Montero and Jian, 1995; Kaplan et al, 1996; Markstahler et al, 1998; Arckens et al, 2000; Soares et al, 2005; Warner et al, 2012). Previous studies in rodents demonstrated that visual stimulation induces the expressions of Zif268 and c-Fos proteins at the peak level within 1 h from stimulus onset (Worley et al, 1991; Zangenehpour and Chaudhuri, 2002), suggesting that input-driven gene activation in V1 reaches the maximum level within a short period of time.…”

“…In the marmoset vision research, there have been debates whether ocular dominance columns (ODCs) exist (Sengpiel et al, 1996; Markstahler et al, 1998; Chappert-Piquemal et al, 2001; Roe et al, 2005) or not exist (Spatz, 1979, 1989; McLoughlin and Schiessl, 2006; Valverde Salzmann et al, 2012) in adult marmosets. With particular relevance to our study, Markstahler et al (1998) reported columnar ZIF268 immunostaining in layer IVCβ 2 h after monocular visual stimulation following transient (24 h) monocular TTX injection, which they called “physiological ODCs.” To investigate the visually evoked gene expression in primates, marmoset V1 is potentially a very good model.…”

A simpler primate brain: the visual system of the marmoset monkey

“…Early work suggested that marmosets lack ODCs in adulthood (Spatz, 1979, 1989; DeBruyn and Casagrande, 1981), although they can be transiently induced by silencing the input from one eye (Markstahler et al, 1998). Functional measurements in adults also suggest weak segregation of ocular dominance (Sengpiel et al, 1996; Roe et al, 2005).…”