The behavioral tractability of the rabbit was exploited and enabled, in the fully awake state, receptive-field analysis of antidromically identified efferent neurons within the vibrissa representation of primary somatosensory cortex (S-1). Efferent neurons studied included ipsilateral corticocortical neurons (C-IC neurons, n = 56) that project to or beyond the second somatosensory cortical area (S-2) and corticofugal neurons of layer 5 (CF-5 neurons, n = 75) and layer 6 (CF-6 neurons, n = 92) that project to and/or beyond the thalamus. 2. An additional class of neurons was studied that was not activated antidromically from any stimulus site, but which responded synaptically to electrical stimulation of the ventrobasal (VB) thalamus with a burst of three or more spikes at frequencies of 600 to greater than 900 Hz. Most of these neurons also responded synaptically to stimulation of S-2. The action potentials of these neurons were much shorter (mean = 0.43 ms), than those of efferent neurons (mean = 0.98 ms). Such properties have been associated with interneurons found throughout the central nervous system, and these neurons are thereby referred to as suspected interneurons (SINs). Although SINs were found at all cortical depths, a strong peak in the distribution occurred just superficial to the peak in the distribution of CF-5 neurons. Most SINs located within this peak responded to deflection of only a single vibrissa. In contrast, SINs located in layer 6 and in layer 2-3 responded to deflection of many vibrissae (median = 11.0 and 5.5 vibrissae, respectively). In addition, SINs of layer 6 and layer 2-3 had significantly longer synaptic latencies to stimulation of VB thalamus than did SINs located at intermediate cortical depths. 3. The properties of efferent neurons and SINs differed considerably. Efferent neurons never responded to stimulation of VB thalamus with the high-frequency burst of spikes characteristic of SINs. Although greater than 70% of CF-6, CF-5 and C-IC neurons had receptive fields that were directionally selective, only 20% of SINs showed any degree of directional selectivity. Furthermore, SINs showed both much lower angular thresholds to vibrissa deflection and a much greater ability to follow high-stimulus frequencies than was seen in efferent neurons. The spontaneous firing rates of SINs had a mean value of 16.5 spikes/s, which was the highest seen in any population within S-1. 4. CF-5 neurons had a number of properties which contrasted with those of both CF-6 and C-IC neurons.(ABSTRACT TRUNCATED AT 400 WORDS)
