1. We have recently demonstrated that reversible, cooling-induced inactivation of the face motor cortex results in a severe impairment in the ability of monkeys (Macaca fascicularis) to perform a tongue-protrusion task but produces only relatively minor effects on the performance of a biting task by the same monkeys. To establish a neuronal correlate for these different behavioral relations, the present study has detailed the afferent input and intracortical microstimulation (ICMS)-defined output features of a population of face motor cortical neurons, and in a subsequent study we have documented the activities of the same population of neurons during the performance of the tongue-protrusion and biting tasks. 2. Of the 231 single neurons recorded within the face motor cortex, 163 were located at sites from which ICMS (less-than-or-equal-to 20-mu-A) could evoke tongue movements (i.e., "tongue-MI" sites) at the lowest threshold for eliciting orofacial movements. The remainder were located at sites from which ICMS evoked jaw movements ("jaw-MI" sites), face movements ("face-MI" sites), or at a few sites, tongue movements and, at the same threshold intensity, either a jaw movement or a facial movement. 3. We confirmed the general organizational features of the face motor cortex that have been defined in previous studies, but we documented in detail the organizational features for tongue-MI. Thus we found that tongue movements were well represented, whereas jaw-closing movements were poorly represented; the representations for face, jaw, and tongue movements were overlapped; the same ICMS-evoked tongue movement could be multiply represented within tongue-MI; tongue-MI was characterized by a prominent input from superficial mechanosensory afferents, whereas there was little evidence for deep input; a close spatial match was found between ICMS-defined motor output and somatosensory afferent input for tongue-MI. 4. A variety of tongue movements could be evoked by ICMS at tongue-MI sites and were categorized into protrusion, retrusion, laterally directed, and other types of tongue movement. Low-threshold (i.e., less-than-or-equal-to 5-mu-A) ICMS-defined tongue-MI sites, which were considered to represent "efferent zones" projecting relatively directly to motoneurons, were reconstructed three dimensionally to provide insights into the spatial organization of tongue-MI. Examples of each of the four low-threshold efferent-zone categories were usually found throughout the ICMS-defined tongue-MI without any apparent preferential distribution. Furthermore, different low-threshold efferent-zone categories had close spatial relationship to each other in cortex. The closely timed activation of groups of different efferent zones within any part of tongue-MI could potentially contribute to the generation of more complex tongue movements. In the next paper we have provided evidence that these different efferent zones are recruited during the tongue-protrusion task. 5. The types of movements evoked by ICMS at jaw-MI sites principally involved jaw opening, and to a much lesser extent, jaw closing; some of these movements exhibited horizontally directed vector components to the movement. Although most of the mechanosensory afferent input to neurons at tongue-MI sites came from superficial receptors in the tongue dorsum, only one neuron within jaw-MI received such an input. A greater proportion of neurons within jaw-MI than tongue-MI received a deep input or an input from afferents supplying periodontal tissues. 6. These differences in input and output properties of neurons at jaw-MI and tongue-MI sites provide further evidence for a functional dichotomy for these two regions within the face motor cortex, and further support for this view is forthcoming from the next paper, which has documented the activities of jaw-MI and tongue-MI neurons during two different orofacial movements, a tongue-protrusion task and a biting task.
