Functional properties of single neurons in the primate face primary somatosensory cortex. I. Relations with trained orofacial motor behaviors.

1. We have demonstrated recently that reversible, cooling-induced inactivation of the face primary somatosensory cortex (SI) severely impairs the successful performance of a tongue-protrusion task but has relatively minor effects on the performance of a biting task. In an attempt to establish a neuronal correlate for these different behavioral relations, the present study was initiated to document the mechanoreceptive field properties of a population of face SI neurons and their activity during the tongue-protrusion and biting tasks. 2. Within SI, the representation of the face was found immediately lateral to that of the hand, and there was a clear somatotopic pattern of organization within face SI: the periorbital or nose region was located most medially in the face SI, then followed laterally in sequence the representation of the upper lip, lower lip, and intraoral area. A mechanoreceptive field (RF) was identified for 253 neurons, which included 162 "lip RF" neurons receiving mechanosensitive afferent inputs from the upper lip, lower lip, or both; 72 "tongue RF" neurons that received mechanosensitive afferent inputs from the tongue; 11 "periodontium RF" neurons receiving periodontal inputs; and 8 neurons that received inputs from other orofacial regions. 3. Nearly all (249/253) of the face SI neurons responded to light tactile stimuli, and most of them received contralateral inputs (78%) and showed a rapidly adapting (RA) response to tactile stimulation (82%). There was no significant difference in the ratio of slowly adapting (SA) to RA neurons in areas 3b and 1. 4. For 193 neurons studied in one or both of the orofacial tasks, 113 were found, on the basis of histological reconstruction, to be distributed in area 1, 61 in area 3b, and 19 in area 2. 5. The firing rate of most tongue RF (79% of 56) neurons and lip RF (60% of 93) neurons tested was significantly altered during the tongue-protrusion task. Only some (14% of 36 tongue RF neurons and 34% of the 92 lip RF neurons tested) showed a significant change in firing rate during the biting task. Three of 7 periodontium RF neurons studied in the tongue-protrusion task altered their firing rate and 5 of 10 altered their firing rate during the biting task. 6. Most of the 116 face SI neurons studied during both tasks exhibited a preferential relation to the tongue-protrusion task as distinct from the biting task, and none showed task-related activity during the biting task only.(ABSTRACT TRUNCATED AT 400 WORDS)