EFFERENT NEURONS AND SUSPECTED INTERNEURONS IN MOTOR CORTEX OF THE AWAKE RABBIT - AXONAL PROPERTIES, SENSORY RECEPTIVE-FIELDS, AND SUBTHRESHOLD SYNAPTIC INPUTS

1. Properties of antidromically identified efferent neurons within the cortical representation of the vibrissae, sinus hairs, and philtrum were examined in motor cortex of fully awake adult rabbits. Efferent neurons were tested for both receptive held and axonal properties and included callosal(CC) neurons (n = 31), ipsilateral corticocortical (C-IC) neurons (n = 34) that project to primary somatosensory cortex (S-1), and corticofugal neurons of layer 5 (CF-5) (n = 33) and layer 6 (CF-6) (n = 32) that project to and/or beyond the thalamus. Appropriate collision tests demonstrated that substantial numbers of corticocortical efferent neurons project an axon to both the corpus callosum and to ipsilateral S-l. 2. Suspected interneurons (SINs, n = 37) were also studied. These neurons were not activated antidromically from any stimulus site but did respond synaptically to electrical stimulation of the ventrolateral (VL) thalamus and/or S-l with a burst of three or more spikes at frequencies from 600 to >900 Hz. All of these neurons also responded synaptically to stimulation of the corpus callosum. The action potentials of these neurons were much shorter in duration (mean = 0.48 ms), than those of efferent neurons (mean = 0.90 ms). 3. CF-5 neurons differed from CC, C-IC, and CF-6 neurons in their spontaneous firing rates, axonal properties, and receptive held properties. Whereas CF-5 neurons had a mean spontaneous firing rate of 4.1 spikes/s, CC, C-IC, and CF-6 neurons all had mean values of (1 spike/s. Axonal conduction velocities of CF-5 neurons were much higher (mean = 12.76 mis) than either CC (1.47 mis), C-IC (0.97 m/s), or CF-6 (mean = 1.96 m/s) neurons. A decrease in antidromic latency (the ''supernormal'' period) followed a single prior impulse in most CC, C-IC, and CF-6 neurons but was minimal or absent in CF-5 neurons. Although all but two CF-5 neurons responded to peripheral sensory stimulation, many CC (35%), C-IC (59%), or CF-6 (66%) neurons did not. CC, CF-5, 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. 4. Sensory receptive fields of neurons in motor cortex were considerably larger than those observed in S-l but were similar in size to those seen in secondary somatosensory cortex (S-2). Receptive field size, however, was strongly related to efferent destination. Receptive held 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 (median = <14 hairs). In contrast, CF-5 neurons and SINs responded to a median of >25 hairs. Ipsilateral responses were seen in 19 of 112 neurons tested and were found predominantly in SINs(6/27) and CF-5 neurons (8/21). 5. The properties of efferent neurons and SINs differed considerably. The spontaneous firing rates of SINs had a mean value of 10.9 spikes Is, which was the highest seen in any population within motor cortex. All SINs were driven by peripheral stimulation. As noted above, SINs had large receptive fields, and none were directionally selective. In contrast, some members of each efferent population 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) had higher axonal conduction velocities and higher spontaneous firing rates and showed less of a supernormal decrease in antidromic latency than did superficial CC neurons. However, CF-5 neurons