Control of oro-facio-lingual movements by the substantia nigra pars reticulata: High-frequency electrical microstimulation and GABA microinjection findings in rats

To provide direct evidence for substantia nigra pars reticulata (SNr) control of oro-facio-lingual muscle activity, high-frequency electrical microstimulation (mainly trains of 20, 333-Hz cathodal pulses at 40-60μA) and GABA microinjection (1-5μl of 10mM GABA in saline) were carried out using a three-barreled microelectrode at the same SNr site in lightly anesthetized, chronically decorticated rats (n=39). Decortication eliminated the possibility that SNr microstimulation might activate corticofugal fibers descending in the adjoining cerebral peduncle. When the most ventral layer of the SNr was approached, high-amplitude electromyographic (EMG) activity of up to 6 mV with a distinctive waveform appeared synchronously with electrical stimuli in the anterior digastric, masseter, genioglossus, and levator labii superioris muscles. This EMG activity was evoked bilaterally, with an ipsilateral predominance. Eye movements, mostly rotation of the eyeball vertically down in the orbit, were noted. Infrequent blinking was also noted. Histologic examination localized the effector site to the middle third of the mediolateral extent of the caudal SNr corresponding to between 5.8mm (level of the oculomotor nerve) and 6.5mm (caudal end of the SNr) caudal to bregma; and to the ventralmost peripeduncular region of the SNr corresponding to 7.7mm to 8.0mm beneath the cortical surface. We referred to this site as the substantia nigra pars reticulata oro-facio-lingual (SNr-ofl) region. GABA injection produced tonic EMG discharge with consistent amplitude in all of the four muscles studied. The GABA effect was negated by a preceding microinjection of the GABA-A receptor antagonist bicuculline, whereas saline control injection had no effect. Changes in amplitude of evoked EMG activity according to location of the stimulating microelectrode reflected somatotopic organization of the SNr-ofl region. This extremely localized electrical and receptor microstimulation in the SNr produced synchronized powerful contraction of jaw, tongue, and facial muscles with different neural innervation. These findings advance our understanding of the mechanisms of the SNr concerning oro-facio-lingual movements.