Organization of the primate face motor cortex as revealed by intracortical microstimulation and electrophysiological identification of afferent inputs and corticobulbar projections

Abstract

1. The technique of intracortical microstimulation (ICMS), supplemented by single-neuron recording, was used to carry out an extensive mapping of the face primary motor cortex. The ICMS study involved a total of 969 microelectrode penetrations carried out in 10 unanesthetized monkeys (Macaca fascicularis). 2. Monitoring of ICMS-evoked movements and associated electromyographic (EMG) activity revealed a general pattern of motor cortical organization. This was characterized by a representation of the facial musculature, which partially enclosed and overlapped the rostral, medial, and caudal borders of the more laterally located cortical regions representing the jaw and tongue musculatures. Responses were evoked at ICMS thresholds as low as 1 microA, and the latency of the suprathreshold EMG responses ranged from 10 to 45 ms. 3. Although contralateral movements predominated, a representation of ipsilateral movements was found, which was much more extensive than previously reported and which was intermingled with the contralateral representations in the anterior face motor cortex. 4. In examining the fine organizational pattern of the representations, we found clear evidence for multiple representation of a particular muscle, thus supporting other investigations of the motor cortex, which indicate that multiple, yet discrete, efferent microzones represent an essential organizational principle of the motor cortex. 5. The close interrelationship of the representations of all three muscle groups, as well as the presence of a considerable ipsilateral representation, may allow for the necessary integration of unilateral or bilateral activities of the numerous face, jaw, and tongue muscles, which is a feature of many of the movement patterns in which these various muscles participate. 6. In six of these same animals, plus an additional two animals, single-neuron recordings were made in the motor and adjacent sensory cortices in the anesthetized state. These neurons were electrophysiologically identified as corticobulbar projection neurons or as nonprojection neurons responsive to superficial or deep orofacial afferent inputs. The rostral, medial, lateral, and caudal borders of the face motor cortex were delineated with greater definition by ICMS and these electrophysiological procedures than by cytoarchitectonic features alone. We noted that there was an approximate fit in area 4 between the extent of projection neurons and field potentials anti-dromically evoked from the brain stem and the extent of positive ICMS sites.(ABSTRACT TRUNCATED AT 400 WORDS)

A probabilistic map of the human ventral sensorimotor cortex using electrical stimulation

“…This ordered somatotopy with overlap is consistent with the findings in fMRI, ECoG, and microstimulation in primates. 1,9,21 Similarly, the probability map for speech arrest in the pars opercularis and precentral gyrus fits well with prior results. 18,22 There are a number of limitations to the present study that should be mentioned.…”

“…It seems likely that the spatial scale of clinical stimulation (5 mm) might result in movements closer to the tonic/seizure end of the spectrum, whereas microstimulation (~ 1 mm) may produce finer movements closer to the behavioral end of the spectrum. 8,9,16 Just as in previous human and animal stimulation studies, the observed responses were stereotyped across subjects, allowing for easy classification in most cases.…”

“…6,17 In this popular conception of vSMC organization, there is a discretely ordered progression of representations for the lips, jaw, tongue, and pharynx/ larynx, respectively, along the dorsal-to-ventral orientation of the central sulcus. More contemporary electrical stimulation 8,9,15,23 and functional MRI (fMRI) 14,21 studies in humans and monkeys have demonstrated that Penfield's original somatotopy holds true in general; however, ECS in individual patients rarely fully recapitulates what was described in those early published maps.…”

Characterization of some morphological parameters of orbicularis oculi motor neurons in the monkey

“…9). This relationship is supported by studies examining the effects of cortical stimulation on the ventral region of M1 which primarily elicits contralateral lower facial movements (Penfield, 1937;Woolsey et al,1952;Woolsey et al, 1979;McGuinness et al, 1980;Huang et al, 1988;Triggs et al, 2005) and longstanding clinical observations which have drawn the association between prominent contralateral lower facial paresis and injury afflicting the lateral peri-central cortex of the cerebral hemisphere (Green, 1938;Symon et al, 1975;Brodal, 1981;Adams et al, 1997). However, it has also been shown that to a lesser extent, OO activation can occur following direct stimulation of M1 (Woolsey et al, 1979;Benecke et al, 1988;Cruccu et al, 1990;Roedel et al, 2001;Sohn et al, 2004;Paradiso et al, 2005) and deficits transpire in OO function following damage to M1 that are less notable than perioral deficits, but are nonetheless detectable (Kojima et al, 1997).…”

Information, information transfer, and information processing

“…We have recently begun investigating the possible role and plasticity of the face sensorimotor cortex in the monkey's acquisition of orofacial motor skills, building on our earlier findings from intracortical microstimulation (ICMS) mapping and recording of neuronal activity in the awake monkey's face MI. The mapping had revealed an extensive representation of the orofacial muscles participating in facial expression and other communicative behaviours as well as in cyclic jaw and tongue movements associated with ingestive behaviours (e.g., licking, mastication, swallowing; Huang et al 1988Huang et al , 1989Martin et al 1999). The cyclic movements can be evoked not only from face MI but also from cortical regions more lateral to face MI (e.g., the "cortical masticatory area," CMA).…”