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The Journal of Neuroscience, November 15, 2000, 20(22):8596-8606

Loss of Presynaptic and Postsynaptic Structures Is Accompanied by Compensatory Increase in Action Potential-Dependent Synaptic Input to Layer V Neocortical Pyramidal Neurons in Aged Rats

Tak Pan Wong¹, Giorgio Marchese¹, Maria Antonietta Casu¹, Alfredo Ribeiro-da-Silva^{1, 2}, A. Claudio Cuello^{1, 2}, and Yves De Koninck¹

¹ Departments of Pharmacology and Therapeutics, and ² Anatomy and Cell Biology, McGill University, Montreal, Quebec, Canada, H3G 1Y6

Reduction in both presynaptic and postsynaptic structures in the aging neocortex may significantly affect functional synaptic properties in this area. To directly address this issue, we combined whole-cell patch-clamp recording of spontaneously occurring postsynaptic currents (PSCs) with morphological analysis of layer V pyramidal neurons in the parietal cortex of young adult (1- to 2-month-old) and aged (28- to 37-month-old) BNxF344 F₁ hybrid rats. Analysis of spontaneous PSCs was used to contrast functional properties of basal synaptic input with structural alterations in the dendritic tree of pyramidal neurons and density of terminals in contact with these cells.

We observed significant changes in a number of morphological parameters of pyramidal neurons in aged rats. These include smaller cell body size and fewer basal dendritic branches (but not of oblique dendrites and dendritic tufts) and spines. Ultrastructural analysis also revealed a lower density of presynaptic terminals per unit length of postsynaptic membrane of labeled pyramidal neurons in the aged brain. This reduction in both presynaptic and postsynaptic elements was paralleled by a significant decrease in frequency of tetrodotoxin-insensitive miniature (action potential-independent) PSCs (mPSCs). The frequency of excitatory and inhibitory mPSCs was reduced to the same extent. In contrast, no significant change was observed in the frequency of spontaneous PSCs recorded in absence of tetrodotoxin (sPSCs), indicating an increase in action potential-dependent (frequency_sPSCs  frequency_mPSCs) input to pyramidal neurons in the aged group. This functional compensation may explain the lack of drastic loss of spontaneous neuronal activity in normal aging.

Key words: aging; dendritic morphometry; electron microscopy; EPSC; IPSC; parietal cortex; patch-clamp; spontaneous synaptic activity

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Copyright © 2000 Society for Neuroscience  0270-6474/00/20228596-11$05.00/0

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