1. Receptive-field properties of antidromically identified efferent neurons within the representation of vibrissae and sinus hairs above the mouth were examined in secondary somatosensory cortex (S-2) of fully awake adult rabbits. Efferent neurons studied included callosal neurons (CC neurons, n = 88), ipsilateral corticocortical neurons (C-IC neurons, n = 5 1) that project to primary somatosensory cortex (S-1), and corticofugal neurons of layer 5 (CF-5 neurons, n = 63) and layer 6 (CF-6 neurons, n = 42) that project to and/or beyond the thalamus. Appropriate collision tests demonstrated that substantial numbers of corticocortical efferent neurons (21 of 113 tested) project an axon to both the corpus callosum and to ipsilateral S-1. 2. Suspected interneurons (SINs, n = 62) were also studied. These neurons were not activated antidromically from any stimulus site but did respond 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-1 and the corpus callosum. The action potentials of these neurons were much shorter (mean, 0.49 ms) than those of efferent neurons (mean, 1.01 ms). 3. CF-5 neurons differed from CC, C-IC, and CF-6 neurons in their spontaneous firing rates, axonal properties, and receptive-field properties. Whereas CF-5 neurons had a mean spontaneous firing rate of 5.7 spikes/s, CC, C-IC, and CF-6 neurons all had mean values of < 1 /s. Axonal conduction velocities of CF-5 neurons were much higher (mean, 11.90 m/s) than either CC (mean, 2.63 m/s), C-IC (mean, 0.86 m/s), or CF-6 (mean, 1.73 m/s) neurons. A decrease in antidromic latency (the "supernormal" period), which was dependent on prior impulse activity, was seen in most CC, C-IC, and CF-6 neurons but was minimal or absent in CF-5 neurons of comparable conduction velocity. Although all CF-5 neurons responded to peripheral sensory stimulation, many CC (52%), C-IC (49%), and CF-6 (55%) neurons did not. CC and CF-6 neurons that did not respond to sensory stimulation had significantly lower axonal conduction velocities and spontaneous firing rates than those that responded to such stimulation. Whereas no CC, C-IC, or CF-6 neuron responded synaptically to callosal stimulation, 43% of CF-5 neurons (and 78% of SINs) did so respond. Similar differences in synaptic responsivity to stimulation of S-1 were seen in these populations. 4. Receptive fields of neurons in S-2 were considerably larger than those observed in S-1, and fewer sustained responses were seen. Receptive-field size, however, was strongly related to efferent destination. Receptive-field size was measured as the number of vibrissae and/or sinus hairs that were encompassed by the receptive field. CC, C-IC, and CF-6 neurons had the smallest receptive fields (medians, 4-6 hairs). In contrast, CF-5 neurons responded to a median of 20-25 hairs, and SINs had the largest receptive fields observed in S-2, responding to a median of 30-35 hairs. Ipsilateral responses were rare and were seen only in some CF-5 (8/42) and CC (3/67) neurons. 5. The properties of efferent neurons and SINs differed considerably. The spontaneous firing rates of SINs had a mean value of 10.6 spikes/s, which was the highest seen in any population within S-2. All SINs were driven by peripheral stimulation. As noted above, SINs had the largest receptive fields seen in S-2, and none were directionally selective. In contrast, a substantial proportion of all efferent populations (40-73%) were directionally selective. In addition, SINs were able to follow considerably higher frequencies of peripheral stimulation than were efferent neurons. 6. The properties of CC and C-IC neurons varied significantly with cortical depth. Deep CC neurons (those found among the CF-5 neurons, presumably in layer 5) had higher axonal conduction velocities, higher spontaneous firing rates and showed less of a supernormal decrease in antidromic latency than did superficial CC neurons. However, CF-5 neurons had even higher axonal conduction velocities and spontaneous firing rates and showed much less of a supernormal decrease in antidromic latency than did the deep CC neurons. Similarly, deep C-IC neurons had higher spontaneous firing rates and showed less supernormality than did superficial C-IC neurons, but their axonal conduction velocities did not vary with cortical depth. 7. The awake rabbit preparation used here was the same as that used in previous studies of V-1 and S-1 to examine receptive-field and axonal properties of corresponding populations of CF-6, CF-5, CC, and C-IC efferent neurons and SINs. Three general points have emerged from comparisons of S-1 and V-1, and these may now be extended to S-2, which has a cytoarchitecture distinct from primary granular cortex: 1) corresponding populations of efferent neurons in S-1, S-2, and V-1 are strikingly similar in their axonal properties, spontaneous firing rates, and receptive-field properties; 2) in S-1, S-2, and V-1 the properties of CC, C-IC, and CF-6 neurons are very similar but differ considerably from those of CF-5 neurons; and 3) SINs of S-1, S-2, and V-1 share numerous functional properties, which differ considerably from those of efferent neurons of these regions. These findings suggest that a common functional plan underlies the operations of sensory neocortex and that efferent analysis may be pivotal to understanding this plan.
