Common synaptic input to the human hypoglossal motor nucleus.

The tongue plays a key role in various volitional and automatic functions such as swallowing, maintenance of airway patency, and speech. Precisely how hypoglossal motor neurons, which control the tongue, receive and process their often concurrent input drives is a subject of ongoing research. We investigated common synaptic input to the hypoglossal motor nucleus by measuring the coordination of spike timing, firing rate, and oscillatory activity across motor units recorded from unilateral (i.e., within a belly) or bilateral (i.e., across both bellies) locations within the genioglossus (GG), the primary protruder muscle of the tongue. Simultaneously recorded pairs of motor units were obtained from 14 healthy adult volunteers using tungsten microelectrodes inserted percutaneously into the GG while the subjects were engaged in volitional tongue protrusion or rest breathing. Bilateral motor unit pairs showed concurrent low frequency alterations in firing rate (common drive) with no significant difference between tasks. Unilateral motor unit pairs showed significantly stronger common drive in the protrusion task compared with rest breathing, as well as higher indices of synchronous spiking (short-term synchrony). Common oscillatory input was assessed using coherence analysis and was observed in all conditions for frequencies up to ∼ 5 Hz. Coherence at frequencies up to ∼ 10 Hz was strongest in motor unit pairs recorded from the same GG belly in tongue protrusion. Taken together, our results suggest that cortical drive increases motor unit coordination within but not across GG bellies, while input drive during rest breathing is distributed uniformly to both bellies of the muscle.

[1]  J. Semmler,et al.  Low-frequency common modulation of soleus motor unit discharge is enhanced during postural control in humans , 2006, Experimental Brain Research.

[2]  E. Fetz,et al.  Synchronization of neurons during local field potential oscillations in sensorimotor cortex of awake monkeys. , 1996, Journal of neurophysiology.

[3]  J. Semmler,et al.  Motor unit discharge and force tremor in skill- and strength-trained individuals , 1998, Experimental Brain Research.

[4]  T. Miles,et al.  Asymmetric activation of motor cortex controlling human anterior digastric muscles during speech and target-directed jaw movements. , 2009, Journal of neurophysiology.

[5]  P. A. Richardson,et al.  Tonically discharging genioglossus motor units show no evidence of rate coding with hypercapnia. , 2010, Journal of neurophysiology.

[6]  Michael A. Nordstrom,et al.  Influence of handedness on motor unit discharge properties and force tremor , 2004, Experimental Brain Research.

[7]  J. Stephens,et al.  Synchronization of motor unit activity during voluntary contraction in man. , 1990, The Journal of physiology.

[8]  J. R. Rosenberg,et al.  A review of recent applications of cross-correlation methodologies to human motor unit recording , 1997, Journal of Neuroscience Methods.

[9]  A. Fuglevand,et al.  Common input to motor neurons innervating the same and different compartments of the human extensor digitorum muscle. , 2004, Journal of neurophysiology.

[10]  C. Christakos,et al.  Coherent motor unit rhythms in the 6-10 Hz range during time-varying voluntary muscle contractions: neural mechanism and relation to rhythmical motor control. , 2008, Journal of neurophysiology.

[11]  C. D. De Luca,et al.  Effects of aging on motor-unit control properties. , 1999, Journal of neurophysiology.

[12]  David R Hillman,et al.  Heterogeneous activity of the human genioglossus muscle assessed by multiple bipolar fine-wire electrodes. , 2003, Journal of applied physiology.

[13]  K. Mosier,et al.  Neural control of tongue movement with respect to respiration and swallowing. , 2001, Critical reviews in oral biology and medicine : an official publication of the American Association of Oral Biologists.

[14]  D. Halliday,et al.  The frequency content of common synaptic inputs to motoneurones studied during voluntary isometric contraction in man. , 1993, The Journal of physiology.

[15]  P. Brown,et al.  Involvement of the sensorimotor cortex in physiological force and action tremor , 2001, Neuroreport.

[16]  T. Sears,et al.  Short‐term synchronization of intercostal motoneurone activity. , 1976, The Journal of physiology.

[17]  L. Adams,et al.  Synchronization of motor unit firing during different respiratory and postural tasks in human sternocleidomastoid muscle. , 1989, The Journal of physiology.

[18]  Shi Zhou,et al.  Motor unit synchronisation is enhanced during slow lengthening contractions of a hand muscle , 2002, The Journal of physiology.

[19]  J. R. Rosenberg,et al.  The unilateral and bilateral control of motor unit pairs in the first dorsal interosseous and paraspinal muscles in man , 1999, The Journal of physiology.

[20]  C. J. Luca Control properties of motor units , 1985 .

[21]  Barry Horwitz,et al.  Functional But Not Structural Networks of the Human Laryngeal Motor Cortex Show Left Hemispheric Lateralization during Syllable But Not Breathing Production , 2009, The Journal of Neuroscience.

[22]  J. Stephens,et al.  Effect of task on the degree of synchronization of intrinsic hand muscle motor units in man. , 1991, Journal of neurophysiology.

[23]  Lemon Rn,et al.  The G. L. Brown Prize Lecture. Cortical control of the primate hand , 1993 .

[24]  R. Miselis,et al.  Dendritic architecture of hypoglossal motoneurons projecting to extrinsic tongue musculature in the rat , 1994, The Journal of comparative neurology.

[25]  E. Fetz,et al.  Short-term synchronization of motor units in human extensor digitorum communis muscle: relation to contractile properties and voluntary control , 2004, Experimental Brain Research.

[26]  Richard S. Snell,et al.  Clinical Neuroanatomy for Medical Students , 1980 .

[27]  Michael A. Nordstrom,et al.  Relationship between motor unit short-term synchronization and common drive in human first dorsal interosseous muscle , 1997, Brain Research.

[28]  J. R. Rosenberg,et al.  Load-independent contributions from motor-unit synchronization to human physiological tremor. , 1999, Journal of neurophysiology.

[29]  R N Lemon,et al.  Modulation of synchrony between single motor units during precision grip tasks in humans , 2002, The Journal of physiology.

[30]  Alexander Adam,et al.  Ordered motor-unit firing behavior in acute cerebellar stroke. , 2006, Journal of neurophysiology.

[31]  J. Rekling,et al.  Hypoglossal motoneurons in newborn mice receive respiratory drive from both sides of the medulla , 2009, Neuroscience.

[32]  N Kakuda,et al.  Common modulation of motor unit pairs during slow wrist movement in man , 1999, The Journal of physiology.

[33]  Madeleine M. Lowery,et al.  Coherence between motor unit discharges in response to shared neural inputs , 2007, Journal of Neuroscience Methods.

[34]  J. R. Rosenberg,et al.  The Fourier approach to the identification of functional coupling between neuronal spike trains. , 1989, Progress in biophysics and molecular biology.

[35]  P. Ellaway,et al.  THE SOURCE AND DISTRIBUTION OF SHORT-TERM SYNCHRONY BETWEEN γ-MOTONEURONES IN THE CAT , 1985 .

[36]  D. Fuller,et al.  Influence of posture and breathing route on neural drive to upper airway dilator muscles during exercise. , 2000, Journal of applied physiology.

[37]  D. Farina,et al.  Fluctuations in isometric muscle force can be described by one linear projection of low‐frequency components of motor unit discharge rates , 2009, The Journal of physiology.

[38]  J. Duffin,et al.  Bilateral synchronisation of respiratory motor output in rats: adult versus neonatal in vitro preparations , 2001, Pflügers Archiv.

[39]  Zeynep Erim,et al.  Journal of Neuroengineering and Rehabilitation Open Access Time and Frequency Domain Methods for Quantifying Common Modulation of Motor Unit Firing Patterns , 2004 .

[40]  Paolo Bonato,et al.  Motor unit recruitment and proprioceptive feedback decrease the common drive. , 2009, Journal of neurophysiology.

[41]  P H Ellaway,et al.  Cumulative sum technique and its application to the analysis of peristimulus time histograms. , 1978, Electroencephalography and clinical neurophysiology.

[42]  W. Z. Rymer,et al.  Evidence of shared, direct input to motoneurons supplying synergist muscles in humans , 1989, Neuroscience Letters.

[43]  R N Lemon,et al.  The G. L. Brown Prize Lecture. Cortical control of the primate hand , 1993, Experimental physiology.

[44]  François G. Meyer,et al.  Coherence at 16-32 Hz can be caused by short-term synchrony of motor units. , 2005, Journal of neurophysiology.

[45]  D. L. Tuck,et al.  Variations in the time course of the synchronization of intercostal motoneurones in the cat , 1982, The Journal of physiology.

[46]  G. Carter Coherence and time delay estimation , 1987, Proceedings of the IEEE.

[47]  T S Miles,et al.  Control of motor units in human flexor digitorum profundus under different proprioceptive conditions , 1997, The Journal of physiology.

[48]  Alexander Adam,et al.  Motor unit control and force fluctuation during fatigue. , 2009, Journal of applied physiology.

[49]  P. Brown,et al.  EEG–EMG, MEG–EMG and EMG–EMG frequency analysis: physiological principles and clinical applications , 2002, Clinical Neurophysiology.

[50]  C. D. De Luca,et al.  Voluntary control of motor units in human antagonist muscles: coactivation and reciprocal activation. , 1987, Journal of neurophysiology.

[51]  W. Smoker,et al.  Hypoglossal Nerve , 1987 .

[52]  C. Christakos,et al.  Occurrence of widespread motor-unit firing correlations in muscle contractions: their role in the generation of tremor and time-varying voluntary force. , 1999, Journal of neurophysiology.

[53]  J. Wessberg,et al.  Organization of motor output in slow finger movements in man. , 1993, The Journal of physiology.

[54]  J. Riggs Distinguishing between extrinsic and intrinsic tongue muscle weakness in unilateral hypoglossal palsy , 1984, Neurology.

[55]  Annie Schmied,et al.  Selective enhancement of motoneurone short-term synchrony during an attention-demanding task , 2000, Experimental Brain Research.

[56]  C. D. De Luca,et al.  Control scheme governing concurrently active human motor units during voluntary contractions , 1982, The Journal of physiology.

[57]  P. Brown Cortical drives to human muscle: the Piper and related rhythms , 2000, Progress in Neurobiology.

[58]  C. Marsden,et al.  Frequency peaks of tremor, muscle vibration and electromyographic activity at 10 Hz, 20 Hz and 40 Hz during human finger muscle contraction may reflect rhythmicities of central neural firing , 1997, Experimental Brain Research.

[59]  François G. Meyer,et al.  Motor-unit coherence and its relation with synchrony are influenced by training. , 2004, Journal of neurophysiology.

[60]  Hartmut Schneider,et al.  Upper airway neuromuscular compensation during sleep is defective in obstructive sleep apnea. , 2008, Journal of applied physiology.

[61]  P H Ellaway,et al.  The source and distribution of short-term synchrony between gamma-motoneurones in the cat. , 1985, Quarterly journal of experimental physiology.

[62]  Carlo J. Deluc CONTROL PROPERTIES OF MOTOR UNITS , 1985 .

[63]  Gary Kamen,et al.  Lateral dominance and motor unit firing behavior , 1992, Brain Research.

[64]  Zeynep Erim,et al.  Common drive of motor units in regulation of muscle force , 1994, Trends in Neurosciences.

[65]  I. Tanaka,et al.  Distribution and medullary projection of respiratory neurons in the dorsolateral pons of the rat , 2006, Neuroscience.