Abstract
Functional sensory and motor areas in the developing mammalian neocortex are formed through a complex interaction of cortically intrinsic mechanisms, such as gene expression, and cortically extrinsic mechanisms such as those mediated by thalamic input from the senses. Both intrinsic and extrinsic mechanisms are believed to be involved in cortical patterning and the establishment of areal boundaries in early development; however, the nature of the interaction between intrinsic and extrinsic processes is not well understood. In a previous study, we used a perinatal bilateral enucleation mouse model to test some aspects of this interaction by reweighting sensory input to the developing cortex. Visual deprivation at birth resulted in a shift of intraneocortical connections (INCs) that aligned with ectopic ephrin A5 expression in the same location ten days later at postnatal day (P) 10. A prevailing question remained: Does visual deprivation first induce a change in gene expression, followed by a shift in INCs, or vice versa? In the present study, we address this question by investigating the neuroanatomy and patterns of gene expression in post-natal day (P) 1 and 4 mice following bilateral enucleation at birth. Our results demonstrate a rapid reduction in dorsal lateral geniculate nucleus (dLGN) size and ephrin A5 gene expression 24-hours post-enucleation, with more profound effects apparent at P4. The reduced nuclear size and diminished gene expression mirrors subtle changes in ephrin A5 expression evident in P1 and P4 enucleated neocortex, 11 and 8 days prior to natural eye opening, respectively. Somatosensory and visual INCs were indistinguishable between P1 and P4 mice bilaterally enucleated at birth, indicating that perinatal bilateral enucleation initiates a rapid change in gene expression (within one day) followed by an alteration of sensory INCs later on (second postnatal week). With these results, we gain a deeper understanding of how gene expression and sensory input together regulate cortical arealization and plasticity during early development.
Highlights
The mammalian neocortex is a complex structure in the central nervous system that contains a unique set of functional and anatomical properties
In this study we used a sensory deprivation model to determine whether deprivation leads to a change in gene expression followed by a remodeling of intraneocortical connections, or vice versa
Previous data led us to hypothesize that acute visual deprivation achieved through bilateral enucleation would first generate a change in cortical gene expression followed by remodeling of sensory intraneocortical connections (INCs) in cortex
Summary
The mammalian neocortex is a complex structure in the central nervous system that contains a unique set of functional and anatomical properties. This structure is responsible for integration of naturally occurring cognitive demands in the everyday environment, including language, decision-making, motivation and sensori-motor processing. Sensory and motor areas are formed in the neocortex through a process called arealization. The mechanisms responsible for cortical area development, or arealization, have been debated for years, with two contradictory models initially emerging: the Protomap and Protocortex hypotheses [1,2]. We begin to unravel ways in which these two hypothetical mechanisms interact within the developing visual system of mice
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