Development of motor maps in rats and their modulation by experience

Abstract

While a substantial literature demonstrates the effect of differential experience on development of mammalian sensory cortices and plasticity of adult motor cortex, characterization of differential experience on the functional development of motor cortex is meager. We first determined when forelimb movement representations (motor maps) could be detected in rats during postnatal development and then whether their motor map expression could be altered with rearing in an enriched environment consisting of group housing and novel toys or skilled learning by training on the single pellet reaching task. All offspring had high-resolution intracortical microstimulation (ICMS)-derived motor maps using methodologies previously optimized for the adult rat. First, cortical GABA-mediated inhibition was depressed by bicuculline infusion directly into layer V of motor cortex and ICMS-responsive points were first reliably detected on postnatal day (PND) 13. Without relying on bicuculline disinhibition of cortex, motor maps emerged on PND 35 and then increased in size until PND 60 and had progressively lower movement thresholds. Second, environmental enrichment did not affect initial detection of responsive points and motor maps in non-bicuculline-treated pups on PND 35. However, motor maps were larger on PND 45 in enriched rat pups relative to pups in the standard housing condition. Rats in both conditions had similar map sizes on PNDs 60, 75, and 90. Third, reach training in rat pups resulted in an internal reorganization of the map in the hemisphere contralateral, but not ipsilateral, to the trained forelimb. The map reorganization was expressed as proportionately more distal (digit and wrist) representations on PND 45. Our data indicate that both environmental enrichment and skilled reach training experience can differentially modify expression of motor maps during development.

Motor Cortex Maturation Is Associated with Reductions in Recurrent Connectivity among Functional Subpopulations and Increases in Intrinsic Excitability

“…In rats, colocalization is observed in a minority of L5 corticospinal neurons when distinct retrograde tracers are injected at the C3 and C7 spinal segments (Akintunde and Buxton, 1992;Wang et al, 2011); such double-labeled neurons were excluded from the current study. This segregation of corticospinal projection patterns is also observed in primates, whereby colocalization of retrograde tracers from upper (C2-C4) and lower (C7-T1) spinal segments is Ͻ4% in corticospinal projections arising from primary motor cortex (He et al, 1993).…”

“…Although the development of corticospinal projections within the spinal cord is well documented (Gribnau et al, 1986;Stanfield, 1992;Meng et al, 2004), little is known with regard to how local network properties within M1 evolve during maturation of the motor system. In adulthood, layer 5 corticospinal neurons of the motor cortex are essential for fine motor control (Whishaw et al, 1993;Piecharka et al, 2005;Anderson et al, 2007;Lemon, 2008;Rosenzweig et al, 2010;Wahl et al, 2014), and the pattern of corticospinal interconnectivity is selectively altered following changes to the motor repertoire (Biane et al, 2012).…”

“…In adulthood, layer 5 corticospinal neurons of the motor cortex are essential for fine motor control (Whishaw et al, 1993;Piecharka et al, 2005;Anderson et al, 2007;Lemon, 2008;Rosenzweig et al, 2010;Wahl et al, 2014), and the pattern of corticospinal interconnectivity is selectively altered following changes to the motor repertoire (Biane et al, 2012). Moreover, corticospinal neurons exhibit changes in dendritic morphology, spine dynamics, and representational motor maps within M1 during the acquisition of new motor skills (Nudo et al, 1996;Kleim et al, 1998;Xu et al, 2009;Yang et al, 2009;Wang et al, 2011;.…”

“…We examined changes in intrinsic circuitry among corticospinal neurons during the time frame of postnatal fine motor development to elucidate neural modifications associated with the emergence of fine motor behavior. We used two subpopulations of corticospinal neurons that project to different levels of the spinal cord and appear to be associated with distinct forelimb behaviors (Brichta et al, 1987;Callister et al, 1987;McKenna et al, 2000;Wang et al, 2011;Tosolini and Morris, 2012). This use of distinct corticospinal subpopulations allowed us to probe the evolving nature of recurrent corticospinal interactions within and across subpopulations during development.…”

Hypergravity within a critical period impacts on the maturation of somatosensory cortical maps and their potential for use-dependent plasticity in the adult

“…Collectively, these findings sustain the view that the first 3 postnatal weeks represent a time window that is critical for the developmental segregation of somatotopic maps. Importantly, forelimb motor maps were first detectable at the end of the second postnatal week (Young et al 2012). Moreover, during rat locomotion development, pivoting predominates during the second half of the first week, crawling during most of the second week, and walking or running by the end of the second week (Altman and Sudarshan 1975).…”