Input–output organization of jaw movement‐related areas in monkey frontal cortex

Abstract

The brain mechanisms underlying mastication are not fully understood. To address this issue, we analyzed the distribution patterns of cortico-striatal and cortico-brainstem axon terminals and the origin of thalamocortical and intracortical fibers by injecting anterograde/retrograde tracers into physiologically and morphologically defined jaw movement-related cortical areas. Four areas were identified in the macaque monkey: the primary and supplementary orofacial motor areas (MIoro and SMAoro) and the principal and deep parts of the cortical masticatory area (CMaAp and CMaAd), where intracortical microstimulation produced single twitch-like or rhythmic jaw movements, respectively. Tracer injections into these areas labeled terminals in the ipsilateral putamen in a topographic fashion (MIoro vs. SMAoro and CMaAp vs. CMaAd), in the lateral reticular formation and trigeminal sensory nuclei contralaterally (MIoro and CMaAp) or bilaterally (SMAoro) in a complex manner of segregation vs. overlap, and in the medial parabranchial and Kölliker-Fuse nuclei contralaterally (CMaAd). The MIoro and CMaAp received thalamic projections from the ventrolateral and ventroposterolateral nuclei, the SMAoro from the ventroanterior and ventrolateral nuclei, and the CMaAd from the ventroposteromedial nucleus. The MIoro, SMAoro, CMaAp, and CMaAd received intracortical projections from the ventral premotor cortex and primary somatosensory cortex, the ventral premotor cortex and rostral cingulate motor area, the ventral premotor cortex and area 7b, and various sensory areas. In addition, the MIoro and CMaAp received projections from the three other jaw movement-related areas. Our results suggest that the four jaw movement-related cortical areas may play important roles in the formation of distinctive masticatory patterns.

Primary motor and sensory cortical areas communicate via spatiotemporally coordinated networks at multiple frequencies

“…The observed interactions between MIo and SIo may be explained by a common source of modulatory activity, such as from the thalamus and not due to direct cortico-cortical communication. There are abundant projections from thalamus to MIo and SIo (11,33), and thalamic neurons have been found to oscillate at 6, 10, and 40 Hz and thus have the potential to generate an oscillatory drive to the cortex in these frequencies (32,34,35). However, oscillations may be initiated in the cortex and propagated to the thalamus, which then sends oscillations back to the cortex, thus increasing the cortico-thalamo-cortical resonance (36).…”

“…Sensorimotor control of oral behaviors is complex, involving the integration of afferent information for moving the tongue and facial muscles. Anatomical connections between MIo and SIo are dense and both areas have bilateral orofacial representations and project to brainstem cranial nerve motor nuclei containing the motoneurons projecting to jaw, facial, and tongue muscles (11,12). These connections provide a substrate for interareal communication between MIo and SIo for the control and learning of orofacial behaviors.…”

Synaptic Transmission From the Supratrigeminal Region to Jaw-Closing and Jaw-Opening Motoneurons in Developing Rats

“…The SupV receives abundant orofacial sensory inputs, including periodontal and spindle afferents (Dessem and Taylor 1989;Jerge 1963;Mizuno 1970;Nishimori et al 1986;Nomura and Mizuno 1985;Shigenaga et al 1989) and descending inputs from the cortical masticatory area (Hatanaka et al 2005;Yasui et al 1985). Retrograde axonal tracing studies have shown that premotor neurons targeting the MoV are present in the SupV (Landgren et al 1986;Mizuno et al 1983;Travers and Norgren 1983;Turman Jr and Chandler 1994a,b).…”

The Ventral Primary Somatosensory Cortex of the Primate Brain: Innate Neural Interface for Dexterous Orofacial Motor Control

“…The bidirectional neural interconnection between the vSI and the ventral primary motor area (vMI) was established in neuroanatomical studies of New [17] and Old World monkeys [15,32]. In one study on the vMI, most neurons respond to light tactile stimulation rather than stimulation to deep tissues, such as the muscle and joint, which suggests the particular importance of tactile input in motor control [33].…”