Neocortical synaptogenesis, aging, and behavior: Lifespan development in the motor-sensory system of the rat

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Abstract

Little evidence presently exists on the development and aging of synaptic contacts and their relationship to behavior, particularly in nonvisual brain areas. To investigate this interrelationship, rats at a series of developmental ages [postnatal day 1 (P1) to P90] were initially examined on a battery of motor tasks. The battery, ranging from simple reflexive tests to tests of complex locomotor capacities, consisted of tactile-induced forelimb placing, chin-induced placing, body righting, climbing an inclined plane, traversing a narrow beam, and keeping up with a revolving wheel. Following completion of the behavioral testing, the animals, together with an additional group of aged (28- to 29-month-old) rats, were killed and their motor-sensory cortex was removed, stained with osmium tetroxide or ethanol phosphotungstic acid (EPTA), and examined under electron microscopy for density of synaptic contacts. Simple motor abilities such as tactile-induced placing was present by the end of the first postnatal week, with locomotor performance reaching a mature level by the end of the third postnatal week, and intermediate task abilities maturing within this range. Paralleling the development of complex locomotor skills was a sharp increase in synaptic density in the molecular layer of the motor-sensory cortex, commencing in the second postnatal week and peaking at P30. After P30 there was a sharp decline in synaptic density as well as a decline in performance on some motor tasks, although these two functions seemed to be occurring independently. There was a continued, but less dramatic synaptic loss evident in the aged rats.

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    In the early development of neural circuits, nodes and edges (neurons and synapses) proliferate until roughly age 2 years in humans. Then, development shifts into a largely regressive process, where the number of nodes remains more or less unchanged, but where a majority (50–60%) of synapses are pruned by adulthood [9–12]. Although synaptic loss may seem uneconomical from an engineering point of view, there are two reasons why it may occur in the brain.

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This research was supported by a grant from the Natural Sciences and Engineering Research Council of Canada to T.L.P. The authors express their appreciation to Ms. Janelle LeBoutillier for her technical assistance.

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