PYRAMIDAL NEURONS IN LAYER-5 OF THE RAT VISUAL-CORTEX .2. DEVELOPMENTOF 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 ha ve stout apical dendrites with terminal tufts, and most of them projec t to the superior colliculus (Larkman and Mason: J Neurosci 10:407, '9 0; Kasper et al.: J Comp Neurol, this issue, 339:459-474). ''Slender/u ntufted'' cells have thinner apical trunks with no obvious terminal tu fts, and a substantial proportion of them project to the contralateral visual cortex. These two types also differ in their intrinsic electro physiological features. In this study we describe the postnatal matura tion of the electrophysiological and synaptic properties of layer 5 py ramidal neurons and relate these findings to the morphological develop ment 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 variou s ages, which were injected with biocytin so that morphological and el ectrophysiological data could be obtained from the same cell. Before P 15, injection of a single cell sometimes stained a cluster of neurons of similar morphology, probably as a result of dye coupling. The incid ence of such clustering and the number of neurons within each cluster decreased with age. There was no obvious difference in electrophysiolo gical properties between cells in clusters and age-matched, noncoupled neurons. From P5, the apical dendrites of neurons could easily be cla ssified as ''thick/tufted'' or ''slender/untufted.'' On average, the r esting potential became more negative, and membrane time 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 slight ly faster time constants than ''slender/untufted'' cells. The current- voltage relations of the neurons became progressively more nonlinear d uring maturation, with both rapid inward rectification and time-depend ent rectification or ''sag'' becoming more prominent. There were also changes in the amplitude and waveform of action potentials, which gene rally approached adult values by 3 weeks of age. Action potential thre shold became more negative, both in absolute terms and relative to the resting membrane potential. Action potentials became larger in peak a mplitude and of shorter duration, with both rise and fall times decrea sing progressively during development. In the adult, neurons of the '' thick/tufted'' type but not ''slender/untufted'' cells can fire charac teristic bursts, consisting of two or more action potentials of virtua lly fixed, short interspike interval, in response to current injection . It was not possible to elicit such bursts from any neurons before P1 5; by P21 all ''thick/tufted'' cells recorded had become bursters. Fro m the earliest age studied (P5) onwards, excitatory postsynaptic poten tials (EPSPs) could be evoked with low-strength stimulation of the whi te matter and surrounding gray matter. The rise time and width at half -amplitude of EPSPs became shorter during postnatal development, but t he changes were not significant if the values were normalized with res pect to the membrane time constant. Inhibitory postsynaptic potentials could not be evoked before P9, even using high stimulus strengths ove r a range of resting potentials and in the presence of agents blocking excitatory transmission.