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

Abstract

Skilled movements rely on sensory information to shape optimal motor responses, for which the sensory and motor cortical areas are critical. How these areas interact to mediate sensorimotor integration is largely unknown. Here, we measure intercortical coherence between the orofacial motor (MIo) and somatosensory (SIo) areas of cortex as monkeys learn to generate tongue-protrusive force. We report that coherence between MIo and SIo is reciprocal and that neuroplastic changes in coherence gradually emerge over a few days. These functional networks of coherent spiking and local field potentials exhibit frequency-specific spatiotemporal properties. During force generation, theta coherence (2-6 Hz) is prominent and exhibited by numerous paired signals; before or after force generation, coherence is evident in alpha (6-13 Hz), beta (15-30 Hz), and gamma (30-50 Hz) bands, but the functional networks are smaller and weaker. Unlike coherence in the higher frequency bands, the distribution of the phase at peak theta coherence is bimodal with peaks near 0°and ±180°, suggesting that communication between somatosensory and motor areas is coordinated temporally by the phase of theta coherence. Time-sensitive sensorimotor integration and plasticity may rely on coherence of local and large-scale functional networks for cortical processes to operate at multiple temporal and spatial scales.S ynchrony between cortical areas has been implicated in neuronal communication and plasticity (1-4). Sensorimotor integration and formation of motor memories during learning are examples wherein effective communication between sensory and motor areas of the cerebral cortex is critical. However, very few studies have investigated coherence between the somatosensory and motor pathways in primates (5-7). These past studies have been confined to upper limb tasks, and none of them looked at changes in coherence during learning. Here, we investigated the synchronous activity between the orofacial primary motor (MIo) and somatosensory (SIo) cortical areas that play important roles in the control of orofacial behaviors (8-10). 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. To investigate cortico-cortical interactions between these areas, we measured coherence of spiking and local field potentials (LFPs) recorded simultaneously from MIo and SIo of the left hemisphere as monkeys learned a simple and controlled tongue protrusion task. Several studies using this behavioral paradigm have reported neuroplasticity and modulation of neuronal activity related to tongue protrusion separatel...

In vivo bone strain and finite element modeling of a rhesus macaque mandible during mastication

“…Comparison of our in vivo ε 1 strain orientations from the lateral (buccal) corpus with those from the work of Hylander (summarized in Fig. 1 of Ross et al, 2016) reveals close similarity between the orientations recorded at our upper lateral gauge site during grape chewing and those reported by Hylander and colleagues during chewing on a wide range of foods. We therefore conclude that our in vivo strain data are similar to those reported elsewhere in independent studies.…”

“…This upper lateral gauge site is the most common (and most easily accessed) location of strain gauge placement for in vivo feeding studies (Hylander, 1979a,b; Ross et al, 2016) and food-type-associated variation in strain orientation at this site in vivo is minimal (Ross et al, 2016). The modeling results presented here suggest that this site might not be the best place to detect variation in in vivo strain regimes associated with variation in food type, especially if food type variation elicits variation in bite point during chewing.…”

“…As part of prior research, the animal had been implanted with microelectrode arrays in the orofacial sensorimotor cortex and head posts in the calvaria for attachment of a halo (Arce-McShane et al, 2014, 2016). Seven 2.7 mm × 10 mm Vitallium cortical bone screws (OFSQ13; 3I Implant Company, West Palm Beach, FL, USA) had been implanted, four in the cranium (two in each zygomatic arch) and three in the mandible (symphysis and anterior corpora) to measure mandible kinematics (Reed and Ross, 2010; Iriarte-Diaz et al, 2011; Ross et al, 2012).…”

“…1). The incision was sutured closed with 4-0 Vicryl with the wires exiting the wound; the wires were secured to the skin overlying the superficial masseter (near the axis of rotation of the mandible; Ross et al, 2016), and radiographs were taken to document the precise position and orientation of the gauges (Fig. 1).…”

“…As reviewed elsewhere (Ross and Iriarte-Diaz, 2014; Ross et al, 2016), the most controlled studies of closely related and sympatric primates do not reveal strong relationships between mandibular cross-sectional geometry and diet (Daegling and McGraw, 2001, 2007). While beam models give accurate estimates of the distribution of dorsoventral bending and transverse and sagittal shear stresses in the mandible, they are not as accurate in predicting reaction force magnitudes and orientations, nor torsional and mediolateral bending stress within the mandible (Porro et al, 2011).…”