Elsevier

Neuroscience

Volume 83, Issue 4, 12 January 1998, Pages 1013-1024
Neuroscience

Postnatal differentiation of firing properties and morphological characteristics in layer V pyramidal neurons of the sensorimotor cortex

https://doi.org/10.1016/S0306-4522(97)00463-6Get rights and content

Abstract

The maturational profile of the firing characteristics of 217 layer V pyramidal neurons of rat sensorimotor cortex, injected with biocytin for morphological reconstruction, was analysed by means of intracellular recordings made between postnatal day (P)3 and 22. Starting from the onset of the second postnatal week, the pyramidal neurons could be differentiated as adapting or non-adapting regular spiking on the basis of the presence or absence of spike frequency adaptation. The percentage of non-adapting regular spiking neurons was very high during the second postnatal week (53%) and progressively decreased with age, concurrently with the appearance of the new class of intrinsically bursting neurons (beginning of the third week) whose percentage progressively increased from 23%, found in P14–P16 rats, to 46% in adult rats. Non-adapting regular spiking neurons were found to share with intrinsically bursting neurons several physiological characteristics comprehending faster action potentials, more prominent effect of anomalous rectification and consistent depolarizing afterpotentials, that differentiated them from the adapting regular spiking neurons. Moreover, intrinsically bursting and non-adapting regular spiking neurons were characterized by a round-shaped distribution of basal dendrites and expanded apical dendritic arborization, that differentiated them from the adapting regular spiking neurons showing a simpler dendritic arborization. These morphological hallmarks were seen in immature intrinsically bursting neurons as soon as they became distinguishable, and in immature non-adapting regular spiking neurons starting from the onset of the second postnatal week.

These findings suggest that a significant subpopulation of immature non-adapting regular spiking neurons are committed to becoming bursters, and that they are converted into intrinsically bursting neurons during the second postnatal week, as soon as the ionic current sustaining the burst firing is sufficiently strong. The faster action potentials in both immature non-adapting regular spiking and intrinsically bursting neurons suggest a higher density of Na+ channels in these neuronal classes: the maturational increase in Na+-current, namely of its persistent fraction, may represent the critical event for the conversion of the non-adapting regular spiking neurons into the intrinsically bursting ones.

Section snippets

Experimental procedures

Wistar rats (both sexes; Charles River) were deeply anaesthetized by means of ether vapour and decapitated, the brain was removed and placed in ice-cold artificial cerebrospinal fluid (ACSF) of the following composition (in mM): NaCl, 126; KCl, 3.5; CaCl2, 2; MgSO4, 2; NaH2PO4, 1.2; NaHCO3, 26; and glucose, 10 (pH 7.3–7.4) bubbled with 95% O2 and 5% CO2. Coronal slices, 400–450 μm-thick, were cut from dorsal frontoparietal cortex using a Vibratome, then transferred to an interface chamber and

Results

The firing characteristics of 217 putative pyramidal neurons recorded in immature rats aged between three and 22 days (P3–P6, 12; P7–P13, 38; P14–P17, 109; P18–P22, 56) and of 70 neurons recorded in adult rats, were evaluated.

Postnatal maturation of firing characteristics and associated properties

As previously reported by McCormick and Prince,[33]during the first postnatal week, neocortical pyramidal neurons were already able to generate trains of APs with a rather high firing frequency. However, in our observations, they displayed an homogeneous behaviour including an early decrease in firing frequency and a tendency to discharge, in response to moderately large depolarizing current pulses, with a limited train of APs. The rather stereotyped firing behaviour observed in early postnatal

Acknowledgements

The study was partially supported by CNR (CN94.00962.04) and by Paolo Zorzi Association for Neuroscience. The authors thank Mrs Maria Teresa Pasquali for editing assistance.

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