EFFERENT NEURONS AND SUSPECTED INTERNEURONS IN S-1 FORELIMB REPRESENTATION OF THE AWAKE RABBIT - RECEPTIVE-FIELDS AND AXONAL PROPERTIES

1. Receptive-field properties of antidromically identified efferent neurons within the cutaneous forelimb representation of primary somatosensory cortex (S-1) were examined in fully awake rabbits. Efferent neurons studied included callosal neurons (CC neurons, n = 52), ipsilateral corticocortical neurons (C-IC neurons, n = 48) that project to or beyond the second somatosensory cortical area (S-2), and corticofugal neurons of layer 5 (CF-5 neurons, n = 97) and layer 6 (CF-6 neurons, n = 59) 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 elctrical stimulation of the ventrobasal (VB) thalamus with a burst of three or more spikes at frequencies of 600 to >900 Hz. Most of these neurons also responded synaptically to stimulation of S-2 and the corpus callosum. The action potentials of these neurons were much shorter (mean = 0.45 ms) than those of efferent neurons (mean = 0.95 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). 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 5.5 spikes/s, CC, C-IC, and CF-6 neurons had mean values of <1/s. Axonal conduction velocities of CF-5 neurons were much higher (mean = 12.92 m/s) than either CC (mean = 2.15 m/s), C-IC (mean = 1.31 m/s), or CF-6 (mean = 2.53 m/s) neurons. A decrease in antidromic latency (the 'supernormal' period) that was dependent on prior impulse activity was seen in the great majority of CC, C-IC, and CF-6 neurons but was either minimal or absent in CF-5 neurons of comparable conduction velocity. A higher proportion of CF-5 neurons (98%) responded to peripheral sensory stimulation that did either CC (75%), C-IC (71%), or CF-6 (51%) neurons. CF-6 and C-IC neurons that did not respond to sensory stimulation had significantly lower axonal conduction velocities and spontaneous firing rates that those that responded to such stimulation. 4. Cutaneous receptive fields were seen in most neurons that could be driven by peripheral stimulation. Cutaneous receptive fields of CF-5 neurons were larger than those of CC, C-IC, and CF-6 neurons that were located on equivalent portions of the forelimb. In addition to neurons with cutaneous receptive fields, neurons with exclusively joint and/or muscle receptive fields were also found throughout the 'cutaneous' forelimb representation of S-1. Such neurons were found in the same penetration and often immediately adjacent to neurons responsive to cutaneous input. Most CC, C-IC, and CF-6 neurons that did respond to peripheral stimulation had cutaneous receptive fields. In contrast, most CF-5 neurons were driven only by manipulation of joints and/or muscles, and the joint/muscle yielding a response often lay proximal to the cutaneous receptive fields seen in the same penetration. In addition to the response elicited by such proximal joint/muscle manipulation, many such neurons were inhibited by cutaneous stimulation on more distal portions of the forelimb (regions of the forelimb that included the cutaneous receptive fields of nearby neurons). Many joint/muscle neurons responded with excitation to one limb position and with inhibiton to the opposing limb position. 5. 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. The spontaneous firing rates of SINs had a mean value of 14.7 spikes/s, which was the highest seen in any population within S-1. All SINs were driven by peripheral stimulation, and 94% had cutaneous receptive fiels. The receptive fields of SINs were larger that those of CC, C-IC, and CF-6 neurons, and SINs that responed synaptically to callosal stimulation had much larger receptive fields than those that did not. SINs were able to follow higher frequencies of peripheral stimulation than were efferent neurons. 6. The present single-unit investigation is largely limited to the cutaneous representation of the forelimb. Additional experiments utilized high-density multiple-unit mapping procedures to delineate this area. Separate from but totally encircled by cutaneous S-1, a small region was found in which cells responded only to manipulation of deep tissue.