Semi-Natural Rearing Conditions Alter the Trajectory of Sensorimotor Cortical Development: Functional Connectivity and Behavior

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The developing neocortex is highly malleable. Early experience tunes neural systems to match an organism’s environmental context, allowing the organism to generate adaptive behavior necessary for survival, growth, and reproduction in a changing environment. For decades, paradigms of sensory deprivation and enrichment have been used to show how early sensory input dramatically alters the connectivity and functional organization of primary sensory areas in the neocortex. How these changes in sensory input lead to changes in motor output, and how the developmental trajectory is altered to produce these changes, is unknown. Further, there are few studies that examine how differences in motor opportunities (affordances), particularly those available in large three-dimensional spaces, impact the motor system. We address this issue by rearing rats in a dynamic semi-natural environment 3000 times the size of standard laboratory cages, and quantifying changes in the connectivity and functional organization of motor cortex, and subsequent behavior, at different developmental milestones. In the current proposal, we seek to elucidate what and when specific modifications are made to motor cortex due to variations in the early postnatal environment. We will do this by comparing the emergence of sensorimotor behaviors between laboratory and semi-naturally reared rats, quantifying differences in when behavioral milestones are reached, how well animals accomplish sensorimotor tasks, and what strategies they use to do so. Following behavioral assays, we will examine differences in the intrinsic connectivity (microcircuitry) and organization of primary motor cortex (M1), assessing the distribution and density of connections between movement representations within M1. Additionally, we will examine the emergence of movement representations of different body parts within M1 at different developmental time points using intracortical microstimulation techniques. Finally, we will quantify differences in the macrocircuitry of M1, examining connectivity with other cortical fields within and across hemispheres as well as with subcortical structures. This is the first study that rears laboratory animals in a large and dynamic wild-type environment to systematically address how early experience impacts the development of motor areas of the cortex and the coordinated behaviors that the brain generates.