On the Role of the Pontine Brainstem in Vocal Pattern Generation: A Telemetric Single-Unit Recording Study in the Squirrel Monkey

In a recent study, we localized a discrete area in the ventrolateral pontine brainstem of squirrel monkeys, which seems to play a role in vocal pattern generation of frequency-modulated vocalizations. The present study compares the neuronal activity of this area with that of three motoneuron pools involved in phonation, namely the trigeminal motor nucleus, facial nucleus, and nucleus ambiguus. The experiments were performed in freely moving squirrel monkeys (Saimiri sciureus) during spontaneous vocal communication, using a telemetric single-unit recording technique. We found vocalization-related activity in all motoneuron pools recorded. Each of them, however, showed a specific profile of activity properties with respect to call types uttered, syllable structure, and pre-onset time. Different activity profiles were also found for neurons showing purely vocalization-correlated activity, vocalization- and mastication-correlated activity, and vocalization- and respiration-correlated activity. By comparing the activity properties of the proposed vocal pattern generator with the three motoneuron pools, we show that the pontine vocalization area is, in fact, able to control each of the three motoneuron pools during frequency-modulated vocalizations. The present study thus supports the existence of a vocal pattern generator for frequency-modulated call types in the ventrolateral pontine brainstem.

[1]  J. Abbs,et al.  Musculotopic organization of the facial motor nucleus in macaca fascicularis: A morphometric and retrograde tracing study with cholera toxin B‐HRP , 1990, The Journal of comparative neurology.

[2]  C. Hinrichsen,et al.  Localization of laryngeal motoneurons in the rat: Morphologic evidence for dual innervation? , 1981, Experimental Neurology.

[3]  N. Mizuno,et al.  Representation of the masticatory muscles in the motor trigeminal nucleus of the macaque monkey , 1981, Neuroscience Letters.

[4]  U. Jürgens,et al.  Common input of the cranial motor nuclei involved in phonation in squirrel monkey , 1987, Experimental Neurology.

[5]  J. Boudreau,et al.  Single unit analysis of cat superior olive S segment with tonal stimuli. , 1966, Journal of neurophysiology.

[6]  U. Jürgens,et al.  Cerebral representation of vocalization in the squirrel monkey , 1970, Experimental Brain Research.

[7]  B. Nail,et al.  On the location and size of laryngeal motoneurons in the cat and rabbit , 1984, The Journal of comparative neurology.

[8]  U. Jürgens.  Localization of a pontine vocalization-controlling area. , 2000, The Journal of the Acoustical Society of America.

[9]  N. Mizuno,et al.  A light and electron microscopic study of premotor neurons for the trigeminal motor nucleus , 1983, The Journal of comparative neurology.

[10]  D. Hopkins,et al.  Viscerotopic representation of the upper alimentary tract in the medulla oblongata in the rat: The nucleus ambiguus , 1987, The Journal of comparative neurology.

[11]  M. Antal,et al.  The projections of the midbrain periaqueductal grey to the pons and medulla oblongata in rats , 2001, The European journal of neuroscience.

[12]  U. Jürgens,et al.  Effects of laryngeal nerve transection on squirrel monkey calls , 1978, Journal of comparative physiology.

[13]  N. Mizuno,et al.  Topographical representation of masticatory muscles in the motor trigeminal nucleus in the rabbit: A HRP study , 1978, Neuroscience Letters.

[14]  P. Sawchenko,et al.  Dorsal medullary pathways subserving oromotor reflexes in the rat: Implications for the central neural control of swallowing , 2000, The Journal of comparative neurology.

[15]  P. Gannon,et al.  A specialized innervation of the tensor tympani muscle inMacaca fascicularis , 1987, Brain Research.

[16]  Y Q Li,et al.  Premotor neurons for trigeminal motor nucleus neurons innervating the jaw‐closing and jaw‐opening muscles: Differential differential in the lower brainstem of the rat , 1995, The Journal of comparative neurology.

[17]  D. Riche,et al.  Brainstem neurons projecting to the rostral ventral respiratory group (rVRG) in the medulla oblongata of the rat revealed by co-application of NMDA and biocytin , 1998, Brain Research.

[18]  G. C. Thompson,et al.  Identification of stapedius muscle motoneurons in squirrel monkey and bush baby , 1985, The Journal of comparative neurology.

[19]  R. West,et al.  Laryngeal and respiratory activity during vocalization in macaque monkeys. , 1993, Journal of voice : official journal of the Voice Foundation.

[20]  Y. Nakamura,et al.  Generation of rhythmical ingestive activities of the trigeminal, facial, and hypoglossal motoneurons in in vitro CNS preparations isolated from rats and mice. , 1999, Journal of medical and dental sciences.

[21]  U. Jürgens,et al.  Glutamate-induced vocalization in the squirrel monkey , 1986, Brain Research.

[22]  N. Mizuno,et al.  Identification of premotor interneurons which project bilaterally to the trigeminal motor, facial or hypoglossal nuclei: a fluorescent retrograde double-labeling study in the rat , 1993, Brain Research.

[23]  L. Benevento,et al.  An immunocytochemical method for marking microelectrode tracks following single-unit recordings in long surviving, awake monkeys , 1992, Journal of Neuroscience Methods.

[24]  U. Jürgens,et al.  Role of extralaryngeal muscles in phonation of subhuman primates , 1994, Journal of Comparative Physiology A.

[25]  Z. Wollberg,et al.  Tuning properties of auditory cortex cells in the awake squirrel monkey , 2004, Experimental Brain Research.

[26]  R. Klinke,et al.  Processing of binaural stimuli by cat superior olivary complex neurons , 2004, Experimental Brain Research.

[27]  Uwe Jürgens,et al.  Localization of a vocal pattern generator in the pontine brainstem of the squirrel monkey , 2006, The European journal of neuroscience.

[28]  N. Yoshii,et al.  Ambiguus motoneurons discharging closely associated with ultrasonic vocalization in rats , 1982, Brain Research.

[29]  N. Suga,et al.  Peripheral control of acoustic signals in the auditory system of echolocating bats. , 1975, The Journal of experimental biology.

[30]  P. Kahrilas,et al.  Neuronal activity in nucleus ambiguus during deglutition and vocalization in conscious monkeys , 1994, Experimental Brain Research.

[31]  C. Tsuchitani.  Functional organization of lateral cell groups of cat superior olivary complex. , 1977, Journal of neurophysiology.

[32]  U. Häusler.  Vocalization-correlated respiratory movements in the squirrel monkey. , 2000, The Journal of the Acoustical Society of America.

[33]  D. Irvine,et al.  Auditory input to neurons in mesencephalic and rostral pontine reticular formation: an electrophysiological and horseradish peroxidase study in the cat. , 1983, Journal of neurophysiology.

[34]  Y. Sahara,et al.  Bulbar reticular unit activity during food ingestion in the cat , 1982, Brain Research.

[35]  M. Hirano,et al.  Somatotopic representation of the laryngeal motoneurons in the medulla of monkeys. , 1985, Acta oto-laryngologica.

[36]  R. Cruz-Rizzolo,et al.  Cytoarchitecture and musculotopic organization of the facial motor nucleus in Cebus apella monkey , 2004, Journal of anatomy.

[37]  W. Willis,et al.  The efferent projections of the periaqueductal gray in the rat: A Phaseolus vulgaris‐leucoagglutinin study. I. Ascending projections , 1995, The Journal of comparative neurology.

[38]  U. Jürgens,et al.  Role of the periaqueductal grey in vocal expression of emotion , 1979, Brain Research.

[39]  R. Leanderson,et al.  Electromyographic studies of facial muscle activity in speech. , 1971, Acta oto-laryngologica.

[40]  N. Suga,et al.  Laryngeal mechanisms for the emission of CF-FM sounds in the Doppler-shift compensating bat,Rhinolophus ferrumequinum , 2004, Journal of comparative physiology.

[41]  P. Grohrock,et al.  Dual-channel telemetry system for recording vocalization-correlated neuronal activity in freely moving squirrel monkeys , 1997, Journal of Neuroscience Methods.

[42]  D. Hopkins,et al.  Viscerotopic representation of the upper alimentary tract in the rat: Sensory ganglia and nuclei of the solitary and spinal trigeminal tracts , 1989, The Journal of comparative neurology.

[43]  Steffen R. Hage,et al.  Audio–vocal interaction in the pontine brainstem during self‐initiated vocalization in the squirrel monkey , 2006, The European journal of neuroscience.

[44]  Uwe Jürgens,et al.  Telemetric recording of neuronal activity. , 2006, Methods.

[45]  U. Jürgens,et al.  Projections of the ventrolateral pontine vocalization area in the squirrel monkey , 2006, Experimental Brain Research.

[46]  E. Salzen,et al.  Facial expressions in captive squirrel monkeys (Saimiri sciureus). , 1978, Folia primatologica; international journal of primatology.

[47]  N. Lanerolle.  A pontine call site in the domestic cat: Behavior and neural pathways , 1990, Neuroscience.

[48]  The central acoustic tract and audio‐vocal coupling in the horseshoe bat, Rhinolophus rouxi , 2000, The European journal of neuroscience.

[49]  N. Mizuno,et al.  Premotor neurons projecting simultaneously to two orofacial motor nuclei by sending their branched axons. A study with a fluorescent retrograde double-labeling technique in the rat , 1993, Neuroscience Letters.