Anatomical Correlates of Functional Plasticity in Mouse Visual Cortex

Abstract

Much of what is known about activity-dependent plasticity comes from studies of the primary visual cortex and its inputs in higher mammals, but the molecular bases remain largely unknown. Similar functional plasticity takes place during a critical period in the visual cortex of the mouse, an animal in which genetic experiments can readily be performed to investigate the underlying molecular and cellular events. The experiments of this paper were directed toward understanding whether anatomical changes accompany functional plasticity in the developing visual cortex of the mouse, as they do in higher mammals. In normal mice, transneuronal label after an eye injection clearly delineated the monocular and binocular zones of area 17. Intrinsic signal optical imaging also showed monocular and binocular zones of area 17 but revealed no finer organization of ocular dominance or orientation selectivity. In normal animals, single geniculocortical afferents serving the contralateral eye showed great heterogeneity and no clustering consistent with the presence of ocular dominance patches. Growth and elaboration of terminal arbor continues beyond postnatal day 40 (P40), after the peak of the critical period. After prolonged monocular deprivation (MD) from P20 to P60, transneuronal labeling showed that the projection serving the ipsilateral eye was severely affected, whereas the effect on the contralateral eye's pathway was inconsistent. Optical imaging also showed profound effects of deprivation, particularly in the ipsilateral pathway, and microelectrode studies confirmed continued functional plasticity past P40. Reconstruction of single afferents showed that MD from P20 to P40 promoted the growth of the open eye's geniculocortical connections without causing the closed eye's contralateral projection to shrink, whereas MD from P20 to P60 caused an arrest of growth of deprived arbors. Our findings reveal numerous similarities between mouse and higher mammals in development and plasticity, along with some differences. We discuss the factors that may be responsible for these differences.

Delayed plasticity of inhibitory neurons in developing visual cortex

“…cortical surface, corresponding to the approximate limits of layer II/III in mouse visual cortex (18)(19)(20)(21). Cells that were more superficial than 150 m consisted of sparse layer I neurons.…”

Paravalbumin-Containing Interneuron Connectivity and Critical Period Modulation

“…At P26, an age commensurate with a significant degree of morphological plasticity in rodent cortex (Antonini et al, 1999;Chattopadhyaya et al, 2004;Majewska et al, 2006;Valverde, 1971) remained at a similar size across the ages examined, PV bouton areas in layer 4 and 2/3 increased significantly from P26 to P41. These findings suggest that the maturation of PV interneuron circuitry in layers 5/6, 4 and 2/3, parallels the early inside-out development of cortical lamination.…”

“…3B 3 ). By P41, when anatomical plasticity in mouse visual cortex is significantly reduced (Antonini et al, 1999), we observed both excitatory and inhibitory synapses with PV interneuron dendrites ( Fig. 3C 1 and C 3 ).…”

“…These ages were chosen to represent periods of incremental exposure to primary sensory input, as well as developmental time points of decreasing anatomical malleability in mouse visual cortex (Antonini et al, 1999;Majewska and Sur, 2003;Majewska et al, 2006;Valverde, 1971). We examined a total of 108 ultrathin sections, containing 160 (P21), 168 (P26) and 169 (P41) synaptic PV interneuron terminals.…”

“…However, closing one eye for a period of days or weeks (called monocular deprivation) during a defined temporal window shifts the responses of a majority of cells toward the open non-deprived eye (Hubel and Wiesel, 1970). This shift occurs in parallel with a conspicuous alteration of thalamocortical axon and cortical morphology, yet monocular deprivation is only able to produce dramatic changes in either cortical physiology or anatomy during this "critical period" in development (Antonini et al, 1999;Antonini and Stryker, 1996;Katz and Crowley, 2002;LeVay et al, 1978;Valverde, 1971).…”