Orofacial Motor Control Research Articles

The role of cerebellar FOXP1 in the development of motor and communicative behaviors in mice.

The gene FOXP2 is well established for a role in human speech and language; far less is known about FOXP1. However, this related gene has also been implicated in human language development as well as disorders associated with features of autism spectrum disorder (ASD). FOXP1 protein expression has also recently been identified in the cerebellum-a neural structure previously shown to express FOXP2 protein. The current study sought to elucidate the behavioral implications of a conditional knock-out of Foxp1 using an En1-Cre driver, which is active in the entirety of the cerebellum and a subset of neurons in the midbrain and spinal cord, in mice using a test battery including motor tasks associated with cerebellar dysfunction, as well as communicative and autistic-relevant behaviors. Male and female mice with a conditional knock-out (cKO, n = 31) and wildtype littermate controls (WT, n = 34) were assessed for gross and orofacial motor control, motor-coordination learning, locomotion, social behavior, anxiety, auditory processing and expressive vocalizations. Overall results suggest Foxp1 plays a specific role in the development of communicative systems, and phenotypic expression of disruptions may interact with sex. Robust motor deficits associated with Foxp1 protein loss may particularly affect vocalizations based on significant orofacial motor deficits in cKO subjects could also contribute to vocalization anomalies. In summary, the current study provides key insights into the role of Foxp1 in cerebellar function and associated behaviors in mice, with implications for an improved understanding of communicative and motor-based neurodevelopmental disabilities in humans.

Cerebellar Nuclei Receiving Orofacial Proprioceptive Signals through the Mossy Fiber Pathway from the Supratrigeminal Nucleus in Rats.

Proprioception from muscle spindles is necessary for motor function executed by the cerebellum. In particular, cerebellar nuclear neurons that receive proprioceptive signals and send projections to the lower brainstem or spinal cord play key roles in motor control. However, little is known about which cerebellar nuclear regions receive orofacial proprioception. Here, we investigated projections to the cerebellar nuclei from the supratrigeminal nucleus (Su5), which conveys the orofacial proprioception arising from jaw-closing muscle spindles (JCMSs). Injections of an anterograde tracer into the Su5 resulted in a large number of labeled axon terminals bilaterally in the dorsolateral hump (IntDL) of the cerebellar interposed nucleus (Int) and the dorsolateral protuberance (MedDL) of the cerebellar medial nucleus. In addition, a moderate number of axon terminals were ipsilaterally labeled in the vestibular group Y nucleus (group Y). We electrophysiologically detected JCMS proprioceptive signals in the IntDL and MedDL. Retrograde tracing analysis confirmed bilateral projections from the Su5 to the IntDL and MedDL. Furthermore, anterograde tracer injections into the external cuneate nucleus (ECu), which receives other proprioceptive input from forelimb/neck muscles, resulted in only a limited number of ipsilaterally labeled terminals, mainly in the dorsomedial crest of the Int and the group Y. Taken together, the Su5 and ECu axons almost separately terminated in the cerebellar nuclei (except for partial overlap in the group Y). These data suggest that orofacial proprioception is differently processed in the cerebellar circuits in comparison to other body-part proprioception, thus contributing to the executive function of orofacial motor control.

The relevance of the unique anatomy of the human prefrontal operculum to the emergence of speech

Identifying the evolutionary origins of human speech remains a topic of intense scientific interest. Here we describe a unique feature of adult human neuroanatomy compared to chimpanzees and other primates that may provide an explanation of changes that occurred to enable the capacity for speech. That feature is the Prefrontal extent of the Frontal Operculum (PFOp) region, which is located in the ventrolateral prefrontal cortex, adjacent and ventromedial to the classical Broca’s area. We also show that, in chimpanzees, individuals with the most human-like PFOp, particularly in the left hemisphere, have greater oro-facial and vocal motor control abilities. This critical discovery, when combined with recent paleontological evidence, suggests that the PFOp is a recently evolved feature of human cortical structure (perhaps limited to the genus Homo) that emerged in response to increasing selection for cognitive and motor functions evident in modern speech abilities.

A comprehensive analysis of variability in the sulci that define the inferior frontal gyrus in the chimpanzee (Pan troglodytes) brain

AbstractObjectivesIn the human brain, the inferior frontal gyrus (IFG) is comprised of three morphological regions, which include the pars opercularis, pars triangularis, and pars orbitalis. These brains regions are implicated in a number of cognitive and linguistic functions, and the pars opercularis and pars triangularis of the language dominant hemisphere are collectively referred to as Broca's area. Evolution of the morphology of the IFG has been a topic of study in comparative neuroscience.Materials and MethodsUsing magnetic resonance images (MRI) from 294 chimpanzees with known pedigrees, we quantified the folding patterns, surface area, and depth of three sulci and their subdivisions that define the IFG.ResultsChimpanzees show considerable individual variation in IFG sulci. A higher proportion of males and chimpanzees with better orofacial motor control had a bifurcation in the dorsal limb of the fronto‐orbital sulcus. For surface area and depth, chimpanzees with better orofacial motor control had greater leftward asymmetries in surface area and increased gyrification for the fronto‐orbital sulcus and greater rightward biases for the inferior precentral sulcus. Quantitative genetic analyses revealed that the average surface area and depth for three of the five sulci subdivisions were significantly heritable. By contrast, we found no evidence for heritability in asymmetries for any of the sulci.DiscussionThese findings provide context to understanding evolutionary selection for increasing motor, cognitive and linguistic functions among primates, and contribute an essential comparative framework for interpreting IFG evolution in the human lineage.

Vibrotactile Sensitivity of the Glabrous Hand and Perioral Face in Neurotypical Children and Adults

Neural encoding of tactile features by the somatosensory system serves many important perceptual roles, including texture and object discrimination, feedback for precision grip and manipulation, and orofacial motor control for speech, gesture, and eating...

Sulcal Morphology in Cingulate Cortex is Associated with Voluntary Oro-Facial Motor Control and Gestural Communication in Chimpanzees (Pan troglodytes).

Individual differences in sulcal variation within the anterior and mid-cingulate cortex of the human brain, particularly the presence or absence of a paracingulate sulcus (PCGS), are associated with various motor and cognitive processes. Recently, it has been reported that chimpanzees possess a PCGS, previously thought to be a unique feature of the human brain. Here, we examined whether individual variation in the presence or absence of a PCGS as well as the variability in the intralimbic sulcus (ILS) are associated with oro-facial motor control, handedness for manual gestures, and sex in a sample of MRI scans obtained in 225 chimpanzees. Additionally, we quantified the depth of the cingulate sulcus (CGS) along the anterior-posterior axis and tested for association with oro-facial motor control, handedness, and sex. Chimpanzees with better oro-facial motor control were more likely to have a PCGS, particularly in the left hemisphere compared to those with poorer control. Male chimpanzees with better oro-facial motor control showed increased leftward asymmetries in the depth of the anterior CGS, whereas female chimpanzees showed the opposite pattern. Significantly, more chimpanzees had an ILS in the left compared to the right hemisphere, but variability in this fold was not associated with sex, handedness, or oro-facial motor control. Finally, significant population-level leftward asymmetries were found in the anterior portion of the CGS, whereas significant rightward biases were evident in the posterior regions. The collective results suggest that the emergence of a PCGS and enhanced gyrification within the anterior and mid-cingulate gyrus may have directly or indirectly evolved in response to selection for increasing oro-facial motor control in primates.

Quantitative, clinically relevant acoustic measurements of focal embouchure dystonia.

Focal embouchure dystonia impairs orofacial motor control in wind musicians and causes professional disability. A paucity of quantitative measures or rating scales impedes the objective assessment of treatment efficacy. We quantified specific features of focal embouchure dystonia using acoustic measures and developed a metric to assess severity across multiple domains of symptomatic impairment. We recruited 9 brass musicians with and 6 without embouchure dystonia. The following 4 domains of symptomatic dysfunction in focal embouchure dystonia were identified: pitch inaccuracy, sound instability and tremor, sound breaks, and timing variability. Musicians performed sustained tones and sequences, and then acoustic variables within each domain were quantified. A composite brass acoustic severity score composed of these variables was validated against clinical global impressions of severity. Musicians with dystonia performed worse in acoustic domains of pitch inaccuracy (median: dystonia = 100%, control = 62%), instability (median shimmer: dystonia = 3%, control = 2%), and breaks (median: dystonia = 0.34%, control = 0.05%). Tremor in embouchure dystonia was 5 to 8 Hz, intermittent, and variable in amplitude. Rhythmic variability did not differ between groups. Participants with embouchure dystonia had different patterns of impairment across variables. Composite severity scores strongly predicted clinical global impression of severity (R2 = 0.95). Acoustic variables distinguish musicians with embouchure dystonia from controls and reflect different types of symptomatic impairments. Our composite acoustic severity score predicts severity of clinical global impression for musicians with different patterns of symptomatic impairment and may provide a foundation for developing a clinical rating scale. © 2018 International Parkinson and Movement Disorder Society.

Impaired orofacial motor functions on chronic temporomandibular disorders

Because temporomandibular disorders (TMDs) rehabilitation continues to be a challenge, a more comprehensive picture of the orofacial functions in patients with chronic pain is required. This study assessed the orofacial functions, including surface electromyography (EMG) of dynamic rhythmic activities, in patients with moderate-severe signs and symptoms of chronic TMD. It was hypothesized that orofacial motor control differs between patients with moderate-severe chronic TMD and healthy subjects. Seventy-six subjects (46 with TMD and 30 control) answered questionnaires of severity of TMD and chewing difficulties. Orofacial functions and EMG during chewing were assessed.Standardized EMG indices were obtained by quantitative analysis of the differential EMG signals of the paired masseter and temporal muscles, and used to describe muscular action during chewing.TMD patients showed significant greater difficulty in chewing; worse orofacial scores; longer time for free mastication; a less accurate recruitment of the muscles on the working and balancing sides, reduced symmetrical mastication index (SMI) and increased standardized activity during EMG test than healthy subjects. SMI, TMD severity and orofacial myofunctional scores were correlated (P<0.01). Impaired orofacial functions and increased activity of the muscles of balancing sides during unilateral chewing characterized the altered orofacial motor control in patients with moderate-severe chronic TMD. Implications for rehabilitation are discussed.

Oral-diadochokinesis rates across languages: English and Hebrew norms

Oro-facial and speech motor control disorders represent a variety of speech and language pathologies. Early identification of such problems is important and carries clinical implications. A common and simple tool for gauging the presence and severity of speech motor control impairments is oral-diadochokinesis (oral-DDK). Surprisingly, norms for adult performance are missing from the literature. The goals of this study were: (1) to establish a norm for oral-DDK rate for (young to middle-age) adult English speakers, by collecting data from the literature (five studies, N=141); (2) to investigate the possible effect of language (and culture) on oral-DDK performance, by analyzing studies conducted in other languages (five studies, N=140), alongside the English norm; and (3) to find a new norm for adult Hebrew speakers, by testing 115 speakers. We first offer an English norm with a mean of 6.2syllables/s (SD=.8), and a lower boundary of 5.4syllables/s that can be used to indicate possible abnormality. Next, we found significant differences between four tested languages (English, Portuguese, Farsi and Greek) in oral-DDK rates. Results suggest the need to set language and culture sensitive norms for the application of the oral-DDK task world-wide. Finally, we found the oral-DDK performance for adult Hebrew speakers to be 6.4syllables/s (SD=.8), not significantly different than the English norms. This implies possible phonological similarities between English and Hebrew. We further note that no gender effects were found in our study. We recommend using oral-DDK as an important tool in the speech language pathologist's arsenal. Yet, application of this task should be done carefully, comparing individual performance to a set norm within the specific language.Learning outcomes: Readers will be able to: (1) identify the Speech-Language Pathologist assessment process using the oral-DDK task, by comparing an individual performance to the present English norm, (2) describe the impact of language on oral-DDK performance, and (3) accurately detect Hebrew speakers’ patients using this tool.

Somatosensory-Motor Adaptation of Orofacial Actions in Posterior Parietal and Ventral Premotor Cortices

Recent studies have provided evidence for sensory-motor adaptive changes and action goal coding of visually guided manual action in premotor and posterior parietal cortices. To extend these results to orofacial actions, devoid of auditory and visual feedback, we used a repetition suppression paradigm while measuring neural activity with functional magnetic resonance imaging during repeated intransitive and silent lip, jaw and tongue movements. In the motor domain, this paradigm refers to decreased activity in specific neural populations due to repeated motor acts and has been proposed to reflect sensory-motor adaptation. Orofacial movements activated a set of largely overlapping, common brain areas forming a core neural network classically involved in orofacial motor control. Crucially, suppressed neural responses during repeated orofacial actions were specifically observed in the left ventral premotor cortex, the intraparietal sulcus, the inferior parietal lobule and the superior parietal lobule. Since no visual and auditory feedback were provided during orofacial actions, these results suggest somatosensory-motor adaptive control of intransitive and silent orofacial actions in these premotor and parietal regions.

Somatotopic organization of motor areas in Macaca assamensis

The range and complexity of orofacial movements require sophisticated neural circuitries that provide for the coordination and control of these movements and their integration with other motor patterns such as those associated with breathing and walking. This chapter is dedicated to Jim Lund whose many research studies have made major contributions to our knowledge of the role of brainstem and cerebral cortex in orofacial motor control. Our own investigations using intracortical microstimulation (ICMS), cortical cold block, and single neuron recordings have documented that the face primary motor area (MI) and primary somatosensory area (SI) are involved in the control not only of elemental and learned orofacial movements but also of the so-called semiautomatic movements such as mastication and swallowing, the control of which have been largely attributed in the past to brainstem mechanisms. Recent studies have also documented that neuroplasticity of the face sensorimotor cortex is a feature of humans and animals trained in a novel oral motor behavior, and that it reflects dynamic and adaptive events that can be modeled by behaviorally significant experiences, including pain and other alterations to the oral environment. Furthermore, our findings of the disruptive effects of the face sensorimotor cortex cold block indicate that the face MI and SI are also critical in the successful performance of an orofacial motor skill once it is learned. Future studies aimed at the further demonstration of such changes and at their underlying mechanisms and their sequence of appearance in the face sensorimotor cortex and associated cortical areas represent crucial steps for understanding the intracortical processes underlying neuroplasticity related to oral motor learning and adaptation. In view of the role that cortical neuronal ensembles play in motor execution, learning, and adaptation (Nicolelis and Lebedev, 2009), these studies should include the properties and plasticity of neuronal ensembles in several related cortical areas in addition to a specific focus on single neurones or efferent microzones within the face MI or SI. As recently noted (Martin, 2009; Sessle et al., 2007, 2009), such research approaches are also important for developing improved rehabilitative strategies to exploit these mechanisms in humans suffering from chronic orofacial pain or sensorimotor disorders.

Broca’s region: linking human brain functional connectivity data and non‐human primate tracing anatomy studies

Brodmann areas 6, 44 and 45 in the ventrolateral frontal cortex of the left hemisphere of the human brain constitute the anterior language production zone. The anatomical connectivity of these areas with parietal and temporal cortical regions was recently examined in an autoradiographic tract-tracing study in the macaque monkey. Studies suggest strong correspondence between human resting state functional connectivity (RSFC) based on functional magnetic resonance imaging data and experimentally demonstrated anatomical connections in non-human primates. Accordingly, we hypothesized that areas 6, 44 and 45 of the human brain would exhibit patterns of RSFC consistent with patterns of anatomical connectivity observed in the macaque. In a primary analysis, we examined the RSFC associated with regions-of-interest placed in ventrolateral frontal areas 6, 44 and 45, on the basis of local sulcal and gyral anatomy. We validated the results of the primary hypothesis-driven analysis with a data-driven partitioning of ventrolateral frontal cortex into regions exhibiting distinct RSFC patterns, using a spectral clustering algorithm. The RSFC of ventrolateral frontal areas 6, 44 and 45 was consistent with patterns of anatomical connectivity shown in the macaque. We observed a striking dissociation between RSFC for the ventral part of area 6 that is involved in orofacial motor control and RSFC associated with Broca's region (areas 44 and 45). These findings indicate rich and differential RSFC patterns for the ventrolateral frontal areas controlling language production, consistent with known anatomical connectivity in the macaque brain, and suggest conservation of connectivity during the evolution of the primate brain.

Speech, Prosody, and Voice Characteristics of a Mother and Daughter With a 7;13 Translocation AffectingFOXP2

The primary goal of this case study was to describe the speech, prosody, and voice characteristics of a mother and daughter with a breakpoint in a balanced 7;13 chromosomal translocation that disrupted the transcription gene, FOXP2 (cf. J. B. Tomblin et al., 2005). As with affected members of the widely cited KE family, whose communicative disorders have been associated with a point mutation in the FOXP2 gene, both mother and daughter had cognitive, language, and speech challenges. A 2nd goal of the study was to illustrate in detail, the types of speech, prosody, and voice metrics that can contribute to phenotype sharpening in speech-genetics research. A speech, prosody, and voice assessment protocol was administered twice within a 4-month period. Analyses were aided by comparing profiles from the present speakers (the TB family) with those from 2 groups of adult speakers: 7 speakers with acquired (with one exception) spastic or spastic-flaccid dysarthria and 14 speakers with acquired apraxia of speech. The descriptive and inferential statistical findings for 13 speech, prosody, and voice variable supported the conclusion that both mother and daughter had spastic dysarthria, an apraxia of speech, and residual developmental distortion errors. These findings are consistent with, but also extend, the reported communicative disorders in affected members of the KE family. A companion article (K. J. Ballard, L. D. Shriberg, J. R. Duffy, & J. B. Tomblin, 2006) reports information from the orofacial and speech motor control measures administered to the same family; reports on neuropsychological and neuroimaging findings are in preparation.

Variations in the relative speeds of orofacial structures with stuttering severity.

Stuttering can be characterized in part as a disorder in the coordination of different muscle systems. In light of basic aspects of orofacial physiology and development, the speeds of the lips and tongue relative to the jaw may be an important dimension for evaluating motor coordination among persons who stutter (PWS). To test this idea, an electromagnetic system was used to obtain measures of lip, tongue, and jaw speed in 38 adults (29 PWS and 9 normally fluent speakers, NFS) as they repeated a simple speech utterance at a normal rate. Using categorical ratings of stuttering severity, ratios of tongue speed to jaw speed were significantly greater in PWS rated as severe, compared to NFS and other PWS. Significant increases in lower lip-to-jaw and tongue-to-jaw speed ratios with stuttering severity were also reflected in correlation analyses relating speed ratios to a continuous measure of stuttering severity. These trends in speed ratio were related to increases in lower lip and tongue speed and decreases in jaw speed with stuttering severity. Sources of the speed differences are discussed in relation to underlying muscle activity, motor compensation processes in adults, and the development of orofacial motor control in children who stutter.

Projections from the rostral parvocellular reticular formation to pontine and medullary nuclei in the rat: Involvement in autonomic regulation and orofacial motor control

The efferent connections of the rostral parvocellular reticular formation to pontine and medullary nuclei in the rat were studied with anterogradely transported Phaseolus vulgaris leucoagglutinin. Dense innervations from the rostral parvocellular reticular formation were found in the mesencephalic trigeminal nucleus, the supratrigeminal area, the motor trigeminal nucleus, the facial, hypoglossal and parabrachial nuclei and specific parts of the caudal parvocellular reticular formation, including nucleus linearis and the dorsal reticular nucleus of the medulla. The raphe nuclei, nucleus of the solitary tract, inferior olive, dorsal principal sensory, spinal trigeminal nuclei and gigantocellular reticular nucleus and the ventral reticular nucleus of the medulla received moderate projections. In general, the projections from the rostral parvocellular reticular formation were bilateral with an ipsilateral dominance. The dorsal motor vagus and the ambiguus nuclei were not labeled. It is concluded that the rostral parvocellular reticular formation participates in regulation of orofacial motor control and in neural networks for limbic control of metabolic homeostasis.

Quantitative analyses of voluntary orofacial motor control in schizophrenia and tardive dyskinesia

This paper reports the results of an investigation of voluntary control of lip, jaw, and tongue movements in schizophrenic patients with and without tardive dyskinesia. The aims of the study were to determine if voluntary orofacial motor control is disrupted in schizophrenia and to evaluate the relationship between voluntary motor control deficits and selected neurological and behavioral variables. Twenty-two schizophrenic patients and 13 normal control subjects were studied. Of the patients, 11 had moderate to severe TD. Analyses were made of performance on pursuit tracking tasks to evaluate differences between TD and non-TD patients and between medicated and currently unmedicated patients. The results indicated significant group differences in voluntary orofacial motor control. The finding that many non-TD patients exhibited voluntary motor dyscontrol suggests that this may represent a disorder independent of the involuntary dyskinesia. The findings indicated that the level of neuroleptic and/or antiparkinsonian medication was unrelated to the degree of voluntary motor control impairment. The results are discussed in terms of probable neurophysiological mechanisms underlying the motor control deficits in schizophrenia.

Motor somatotopy in the striatum of rat: Manipulation, biting and gait

The objective of this study was to examine the hypothesis of somatotopically organized motor functions in the striatum. In Experiment 1, ibotenate-induced lesions of the rostrolateral striatum in rats produced a transient decrease of ad libitum food intake, a more enduring decrease of body weight, and chronic impairments of food biting, holding of hard food pellets and feeding efficiency, with no apparent alterations of gait balance in a beam walking task. Lesions of the medial striatum had minimal or no reliable effects on any of the measured parameters. In Experiment 2, the motoric effects of ibotenate lesions restricted to either the dorsomedial or the dorsolateral or the ventrolateral regions of the rostral striatum were examined. Lesions of the dorsolateral striatum produced the most deleterious effect on holding postures of the forelimbs, whereas lesions of the ventrolateral striatum maximally affected food biting, feeding efficiency, ad libitum food intake, and body weight. No regional lesions affected gait balance. Dorsomedial striatal lesions did not affect any of the measured parameters. The findings support the hypothesis of a somatotopically organized role of the rostrolateral striatum in orofacial and forelimb motor control.

Response properties of the perioral reflex in parkinson's disease

Analyses of the response magnitudes of the short-latency perioral reflex were made in a group of Parkinson disease patients and control subjects. As a group, the parkinsonian subjects manifested reflex magnitudes which were increased relative to normal. For low-acceleration, mechanical displacements of perioral tissue (<500 cm/s 2), the perioral reflex was not elicited in normal controls. However, such low-acceleration stimuli did elicit the perioral reflex in more than half of the parkinsonian subjects studied. These findings are consistent with earlier findings of increased sensitivity of facial and perioral reflexes associated with disturbances of the basal ganglia. These results contribute to the understanding of specific stimulus-response characteristics of the facial reflex and the role of the basal ganglia in orofacial motor control. The finding of increased sensitivity to mechanical stimuli in Parkinson's disease supports the hypothesis of basal ganglia gating or regulation of afferent information.

Orofacial motor control impairment in Parkinson's disease.

Motor impairments in lip, jaw, and tongue muscles in patients with idiopathic Parkinson's disease (PD) were quantified. These orofacial muscle groups are nonuniformly endowed with muscle afferents, thus permitting evaluation of the hypothesis that certain PD motor symptoms are due to aberrations in muscle afferent function. Tongue muscles, devoid of stretch reflexes, were most impaired, while jaw-closing muscles, with numerous spindles and a monosynaptic stretch reflex, manifested the least impairment. Seemingly, PD motor impairments are independent of fusimotor or muscle afferent dysfunctions.

Labial kinematics during speech in patients with parkinsonian rigidity.

Studies of orofacial motor control in Parkinson's disease (PD) have demonstrated that these subjects may exhibit hypokinesia and bradykinesia, as well as increased muscle tone. Yet the relationship between aberrations of orofacial movement and muscle rigidity remains unclear. Measures of labial muscle rigidity and movement were made for 12 parkinsonian and 9 age-matched control subjects. Displacement amplitude, peak instantaneous velocity, and movement time were evaluated during repetitive syllable productions. The results showed that while mean parkinsonian displacement amplitudes and velocities were lower than the normal control subjects, there was no statistical relationship between labial rigidity and the degree of movement abnormality. It is concluded that while rigidity may play a part in the overall disability, it does not sufficiently explain the labial articulatory difficulties associated with parkinsonism. This is in agreement with the literature on limb rigidity and movement aberrations in PD, suggesting that rigidity and bradykinesia may represent independent pathophysiological phenomena.