EFFECTS OF REVERSIBLE INACTIVATION BY COOLING OF THE PRIMATE FACE MOTOR CORTEX ON THE PERFORMANCE OF A TRAINED TONGUE-PROTRUSION TASK AND A TRAINED BITING TASK

Intracortical microstimulation (ICMS) and surface stimulation studies of primate face motor cortex have shown an extensive representation within face motor cortex devoted to movements of the tongue and face; only a very small representation for jaw-closing movements has ever been demonstrated. These data suggest that face motor cortex plays a critical role in the generation of tongue and facial movements but is less important in the generation of jaw-closing movements. Our aim was to determine whether disruption of primate face motor cortical function would indeed interfere with the generation of tongue movements but would not interfere with the generation of jaw-closing movements. The face motor cortex was reversibly inactivated with the use of cooling in two monkeys that were trained to perform both a tongue-protrusion task and a biting task. Recording of single neuronal activity in the cortex beneath the thermode confirmed the reversible inactivation of the cortex. Each task involved a series of trials in which the monkey was required to produce a preset force level for a 0.5-s force holding period; the monkey received a fruit-juice reward if it successfully completed a task trial. Cooling of the ICMS-defined face motor cortex was achieved bilaterally or, in one experiment, unilaterally by circulating coolant through thermodes placed either on intact dura overlying face motor cortex in both monkeys or directly on the exposed pia in one of the monkeys; thermode temperature was lowered to 3-5°C during cooling. Electromyographic (EMG) recordings were also made from masseter, genioglossus, and digastric muscles. During bilateral cooling of the thermodes on the dura overlying the face motor cortex, there was a significant reduction in the success rates for the performance of the tongue-protrusion task in comparison with control series of trials (i.e., precool and postcool) in which the thermodes were kept at 37°C. Quantitative analyses of force and EMG activity showed that the principal deficit was an inability of each monkey to exert sufficient force with its tongue for a sufficient length of time onto the tongue-protrusion task transducer; this deficit was paralleled by a reduction in the level of genioglossus and digastric EMG activity. At 4 min after commencement of rewarming, task performance had returned to control, precool levels. This depressant effect on the tongue-protrusion task was reproducible on different days, but identical cooling conditions in the same monkeys did not significantly affect the success rates for the performance of the biting task. However, there was a slight but significant reduction for one of the monkeys in the rate of force application during the initial force dynamic phase of the biting task. We found the same effects on success rates when the same cooling experiment was carried out with the thermodes placed directly on the pia overlying face motor cortex. There was a significant reduction in success rates for the performance of the tongue-protrusion task during the cooling in comparison with the control precool and postcool series of trials, but no significant effect was noted on the success rates for the performance of the biting task. Unilateral cooling of face motor cortex through the pia did not result in a significant reduction in success rates for the performance of the tongue-protrusion task in comparison with the control series of trials. Cooling of thermodes placed bilaterally over the ICMS-defined forelimb region of motor cortex did not result in significant effects on the success rates for either task in either monkey. These data suggest an essential role for face motor cortex in the generation and fine control of voluntary tongue movements. In contrast, the data suggest that face motor cortex is not essential for the generation of voluntary jaw-closing movements, although face motor cortex may be of importance in the fine control and modulation of jaw-closing muscle activity.