Pyramidal neurons in layer 5 of the rat visual cortex. II. Development of electrophysiological properties

Two major classes of pyramidal neurons can be distinguished in layer 5 of the adult rat visual cortex. Cells of the “thick/tufted” type have stout apical dendrites with terminal tufts, and most of them project to the superior colliculus (Larkman and Mason: J Neurosci 10:407, '90; Kasper et al.: J Comp Neurol, this issue, 339:459–474). “Slender/untufted” cells have thinner apical trunks with no obvious terminal tufts, and a substantial proportion of them project to the contralateral visual cortex. These two types also differ in their intrinsic electrophysiological features. In this study we describe the postnatal maturation of the electrophysiological and synaptic properties of layer 5 pyramidal neurons and relate these findings to the morphological development and divergence of the two cell types. Living slices were prepared from the visual cortex of rats aged between postnatal day 3 (P3) and young adults and maintained in vitro. Stable intracellular impalements were obtained from a total of 63 pyramidal cells of layer 5 at various ages, which were injected with biocytin so that morphological and electrophysiological data could be obtained from the same cell. Before P15, injection of a single cell sometimes stained a cluster of neurons of similar morphology, probably as a result of dye coupling. The incidence of such clustering and the number of neurons within each cluster decreased with age. There was no obvious difference in electrophysiological properties between cells in clusters and age‐matched, noncoupled neurons. From P5, the apical dendrites of neurons could easily be classified as “thick/tufted” or “slender/untufted.” On average, the resting potential became more negative, and membrane time constant and constant and input resistance decreased with age. Electrophysiological differences between the “thick/tufted” and “slender/untufted” cell types did not become apparent until the third postnatal week, after which the “thick/tufted” cells on average had lower input resistances and slightly faster time constants than “slender/untufted” cells. The current‐voltage relations of the neurons became progressively more nonlinear during maturation, with both rapid inward rectification and time‐dependent rectification or “sag” becoming more prominent. There were also changes in the amplitude and waveform of action potentials, which generally approached adult values by 3 weeks of age. Action potential threshold became more negative, both in absolute terms and relative to the resting membrane potential. Action potentials became larger in peak amplitude and of shorter duration, with both rise and fall times decreasing progressively during development. In the adult, neurons of the “thick/tufted” type but not “slender/untufted” cells can fire characteristic bursts, consisting of two or more action potentials of virtually fixed, short interspike interval, in response to current injection. It was not possible to elicit such bursts from any neurons before P15; by P21 all “thick/tufted” cells recorded had become bursters. From the earliest age studied (P5) onwards, excitatory postsynaptic potentials (EPSPs) could be evoked with low‐strength stimulation of the white matter and surrounding gray matter. The rise time and width at half‐amplitude of EPSPs became shorter during postnatal development, but the changes were not significant if the values were normalized with respect to the membrane time constant. Inhibitory postsynaptic potentials could not be evoked before P9, even using high stimulus strengths over a range of resting potentials and in the presence of agents blocking excitatory transmission. © 1994 Wiley‐Liss, Inc.