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Published in: Experimental Brain Research 1/2006

01-02-2006 | Research Article

Projections of the ventrolateral pontine vocalization area in the squirrel monkey

Authors: Stefanie Hannig, Uwe Jürgens

Published in: Experimental Brain Research | Issue 1/2006

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Abstract

In four squirrel monkeys (Saimiri sciureus), the tracer biotin dextranamine (BDA) was injected into the ventrolateral pons at a site at which injection of the glutamate antagonist kynurenic acid blocked vocalization electrically elicited from the periaqueductal gray (PAG). Anterograde projections could be traced into all cranial motor and sensory nuclei involved in phonation, that is, the nucleus ambiguus, facial, hypoglossal and trigeminal motor nuclei, the motorneuron column in the ventral gray substance innervating the extrinsic laryngeal muscles, the nucleus retroambiguus, solitary tract and spinal trigeminal nuclei. Projections were also found into a number of auditory nuclei, namely the nucleus cochlearis-complex, superior olive, ventral and dorsal nuclei of the lateral lemniscus and inferior colliculus. Furthermore, there were projections into the reticular formation of the lateral and dorsocaudal medulla and lateral pons, into nucleus gracilis, inferior and medial vestibular nuclei, lateral reticular nucleus, ventral raphe, pontine gray, superior colliculus, PAG and mediodorsal thalamic nucleus. Injection of the tracer wheat germ agglutinin-conjugated horseradish peroxidase into the ventrolateral pontine vocalization-blocking area in one animal yielded retrograde labeling throughout the PAG. Injection of BDA into a vocalization-eliciting site of the PAG in another animal yielded projections into the ventrolateral pontine vocalization-blocking area. It is concluded that the ventral paralemniscal area in the ventrolateral pons represents a relay station of the descending periaqueductal vocalization-controlling pathway.
Literature
go back to reference Altschuler SM, Bao X, Bieger D, Hopkins DA, Miselis RR (1989) Viscerotopic representation of the upper alimentary tract in the rat: sensory ganglia and nuclei of the solitary and spinal trigeminal tracts. J Comp Neurol 283:248–268CrossRefPubMed Altschuler SM, Bao X, Bieger D, Hopkins DA, Miselis RR (1989) Viscerotopic representation of the upper alimentary tract in the rat: sensory ganglia and nuclei of the solitary and spinal trigeminal tracts. J Comp Neurol 283:248–268CrossRefPubMed
go back to reference Behrend O, Schuller G (2000) The central acoustic tract and audiovocal coupling in the horseshoe bat, Rhinolophus rouxi. Eur J Neurosci 12:4268–4280PubMedCrossRef Behrend O, Schuller G (2000) The central acoustic tract and audiovocal coupling in the horseshoe bat, Rhinolophus rouxi. Eur J Neurosci 12:4268–4280PubMedCrossRef
go back to reference Brandt HM, Apkarian AV (1992) Biotin-dextran. A sensitive anterograde tracer for neuroanatomic studies in rat and monkey. J Neurosci Meth 45:35–40CrossRef Brandt HM, Apkarian AV (1992) Biotin-dextran. A sensitive anterograde tracer for neuroanatomic studies in rat and monkey. J Neurosci Meth 45:35–40CrossRef
go back to reference Chandler SH, Goldberg LJ (1988) Effects of pontomedullary reticular formation stimulation on the neuronal networks responsible for rhythmical jaw movements in the guinea pig. J Neurophysiol 59:819–832PubMed Chandler SH, Goldberg LJ (1988) Effects of pontomedullary reticular formation stimulation on the neuronal networks responsible for rhythmical jaw movements in the guinea pig. J Neurophysiol 59:819–832PubMed
go back to reference Dressnandt J, Jürgens U (1992) Brain stimulation-induced changes of phonation in the squirrel monkey. Exp Brain Res 89:549–559CrossRefPubMed Dressnandt J, Jürgens U (1992) Brain stimulation-induced changes of phonation in the squirrel monkey. Exp Brain Res 89:549–559CrossRefPubMed
go back to reference Emmers R, Akert K (1963) A stereotaxic atlas of the brain of the squirrel monkey (Saimiri sciureus). University of Wisconsin Press, Madison Emmers R, Akert K (1963) A stereotaxic atlas of the brain of the squirrel monkey (Saimiri sciureus). University of Wisconsin Press, Madison
go back to reference Gergen JA, MacLean PD (1962) A stereotaxic atlas of the squirrel monkey’s brain (Saimiri sciureus), Public Health Service Publication, No. 933, Bethesda/Maryland Gergen JA, MacLean PD (1962) A stereotaxic atlas of the squirrel monkey’s brain (Saimiri sciureus), Public Health Service Publication, No. 933, Bethesda/Maryland
go back to reference Hayakawa T, Takanaga A, Maeda S, Seki M, Yajima Y (2001) Subnuclear distribution of afferents from the oral, pharyngeal and laryngeal regions in the nucleus tractus solitarii of the rat: a study using transganglionic transport of cholera toxin. Neurosci Res 39:221–232CrossRefPubMed Hayakawa T, Takanaga A, Maeda S, Seki M, Yajima Y (2001) Subnuclear distribution of afferents from the oral, pharyngeal and laryngeal regions in the nucleus tractus solitarii of the rat: a study using transganglionic transport of cholera toxin. Neurosci Res 39:221–232CrossRefPubMed
go back to reference Holstege G (1989) Anatomical study of the final common pathway for vocalization in the cat. J Comp Neurol 284:242–252CrossRefPubMed Holstege G (1989) Anatomical study of the final common pathway for vocalization in the cat. J Comp Neurol 284:242–252CrossRefPubMed
go back to reference Jürgens U (1979) Vocalization as an emotional indicator. A neuroethological study in the squirrel monkey. Behaviour 69:88–117PubMed Jürgens U (1979) Vocalization as an emotional indicator. A neuroethological study in the squirrel monkey. Behaviour 69:88–117PubMed
go back to reference Jürgens U (2000) Localization of a pontine vocalization-controlling area. J Acoust Soc Am 108:1393–1396CrossRefPubMed Jürgens U (2000) Localization of a pontine vocalization-controlling area. J Acoust Soc Am 108:1393–1396CrossRefPubMed
go back to reference Jürgens U, Ploog D (1970) Cerebral representation of vocalization in the squirrel monkey. Exp Brain Res 10:532–554CrossRefPubMed Jürgens U, Ploog D (1970) Cerebral representation of vocalization in the squirrel monkey. Exp Brain Res 10:532–554CrossRefPubMed
go back to reference Jürgens U, Pratt R (1979) Role of the periaqueductal grey in vocal expression of emotion. Brain Res 167:367–378PubMedCrossRef Jürgens U, Pratt R (1979) Role of the periaqueductal grey in vocal expression of emotion. Brain Res 167:367–378PubMedCrossRef
go back to reference Jürgens U, Richter K (1986) Glutamate-induced vocalization in the squirrel monkey. Brain Res 373:349–358CrossRefPubMed Jürgens U, Richter K (1986) Glutamate-induced vocalization in the squirrel monkey. Brain Res 373:349–358CrossRefPubMed
go back to reference Jürgens U, Schriever S (1991) Respiratory muscle activity during vocalization in the squirrel monkey. Folia Primatol 56:121–132PubMedCrossRef Jürgens U, Schriever S (1991) Respiratory muscle activity during vocalization in the squirrel monkey. Folia Primatol 56:121–132PubMedCrossRef
go back to reference Kalia M, Mesulam M-M (1980) Brain stem projections of sensory and motor components of the vagus complex in the cat. Laryngeal, tracheobronchial, pulmonary, cardiac, and gastrointestinal branches. J Comp Neurol 193:467–508CrossRefPubMed Kalia M, Mesulam M-M (1980) Brain stem projections of sensory and motor components of the vagus complex in the cat. Laryngeal, tracheobronchial, pulmonary, cardiac, and gastrointestinal branches. J Comp Neurol 193:467–508CrossRefPubMed
go back to reference Kanai T, Wang SC (1962) Localization of the central vocalization mechanism in the brainstem of the cat. Exp Neurol 6:426–434CrossRef Kanai T, Wang SC (1962) Localization of the central vocalization mechanism in the brainstem of the cat. Exp Neurol 6:426–434CrossRef
go back to reference Kirzinger A, Jürgens U (1985) The effects of brain stem lesions on vocalization in the squirrel monkey. Brain Res 358:150–162CrossRefPubMed Kirzinger A, Jürgens U (1985) The effects of brain stem lesions on vocalization in the squirrel monkey. Brain Res 358:150–162CrossRefPubMed
go back to reference Kirzinger A, Jürgens U (1991) Vocalization-correlated single-unit activity in the brain stem of the squirrel monkey. Exp Brain Res 84:545–560CrossRefPubMed Kirzinger A, Jürgens U (1991) Vocalization-correlated single-unit activity in the brain stem of the squirrel monkey. Exp Brain Res 84:545–560CrossRefPubMed
go back to reference Kirzinger A, Jürgens U (1994) Motoneuronal location of external laryngeal and hyoid muscles involved in primate phonation. J Brain Res 35:559–565 Kirzinger A, Jürgens U (1994) Motoneuronal location of external laryngeal and hyoid muscles involved in primate phonation. J Brain Res 35:559–565
go back to reference Larson CR, Sutton D, Lindeman RC (1978) Cerebellar regulation of phonation in rhesus monkey (Macaca mulatta). Exp Brain Res 33:1–18CrossRefPubMed Larson CR, Sutton D, Lindeman RC (1978) Cerebellar regulation of phonation in rhesus monkey (Macaca mulatta). Exp Brain Res 33:1–18CrossRefPubMed
go back to reference MacLean PD (1967) A chronically fixed stereotaxic device for intracerebral exploration with macro- and micro-electrodes. Electroenceph Clin Neurophysiol 22:180–182CrossRefPubMed MacLean PD (1967) A chronically fixed stereotaxic device for intracerebral exploration with macro- and micro-electrodes. Electroenceph Clin Neurophysiol 22:180–182CrossRefPubMed
go back to reference Magoun HW, Atlas D, Ingersoll EH, Ranson SW (1937) Associated facial, vocal and respiratory components of emotional expression: an experimental study. J Neurol Psychopath 17:241–255CrossRef Magoun HW, Atlas D, Ingersoll EH, Ranson SW (1937) Associated facial, vocal and respiratory components of emotional expression: an experimental study. J Neurol Psychopath 17:241–255CrossRef
go back to reference Mesulam M-M (1978) Tetramethyl benzidine for horseradish peroxidase neurohistochemistry: a non-carcinogenic blue reaction product with superior sensitivity for visualizing neural afferents and efferents. J Histochem Cytochem 26:106–117PubMed Mesulam M-M (1978) Tetramethyl benzidine for horseradish peroxidase neurohistochemistry: a non-carcinogenic blue reaction product with superior sensitivity for visualizing neural afferents and efferents. J Histochem Cytochem 26:106–117PubMed
go back to reference Metzner W (1993) An audio-vocal interface in echolocating horseshoe bats. J Neurosci 13:1899–1915PubMed Metzner W (1993) An audio-vocal interface in echolocating horseshoe bats. J Neurosci 13:1899–1915PubMed
go back to reference Metzner W(1996) Anatomical basis for audio-vocal integration in echolocating horseshoe bats. J Comp Neurol 368:252–269CrossRefPubMed Metzner W(1996) Anatomical basis for audio-vocal integration in echolocating horseshoe bats. J Comp Neurol 368:252–269CrossRefPubMed
go back to reference Mori S, Nishimura H, Kurakami C, Yamamura T, Aoki M (1978) Controlled locomotion in the mesencephalic cat: distribution of facilitatory and inhibitory regions within pontine tegmentum. J Neurophysiol 41:1580–1591PubMed Mori S, Nishimura H, Kurakami C, Yamamura T, Aoki M (1978) Controlled locomotion in the mesencephalic cat: distribution of facilitatory and inhibitory regions within pontine tegmentum. J Neurophysiol 41:1580–1591PubMed
go back to reference Pieper F, Jürgens U (2003) Neuronal activity in the inferior colliculus and bordering structures during vocalization in the squirrel monkey. Brain Res 979:153–164PubMedCrossRef Pieper F, Jürgens U (2003) Neuronal activity in the inferior colliculus and bordering structures during vocalization in the squirrel monkey. Brain Res 979:153–164PubMedCrossRef
go back to reference Ploog D (1995) Mutuality and dialogue in nonhuman primate communication. In: Markova I, Graumann CF, Foppa K (eds) Mutualities in dialogue, Cambridge University Press, Cambridge, pp 27–57 Ploog D (1995) Mutuality and dialogue in nonhuman primate communication. In: Markova I, Graumann CF, Foppa K (eds) Mutualities in dialogue, Cambridge University Press, Cambridge, pp 27–57
go back to reference Richter K, Jürgens U (1986) A comparative study on the elicitability of vocalization by electrical brain stimulation, glutamate, aspartate and quisqualate in the squirrel monkey. Neurosci Lett 66:239–244CrossRefPubMed Richter K, Jürgens U (1986) A comparative study on the elicitability of vocalization by electrical brain stimulation, glutamate, aspartate and quisqualate in the squirrel monkey. Neurosci Lett 66:239–244CrossRefPubMed
go back to reference Sakamoto T, Wada K, Yamanaka Y, Shiba K, Nakajima Y (1993) Effects of microinjection of a GABA antagonist into the periaqueductal gray upon electrically-induced vocalization in decerebrate cats. Neurosci Res 18:235–240PubMedCrossRef Sakamoto T, Wada K, Yamanaka Y, Shiba K, Nakajima Y (1993) Effects of microinjection of a GABA antagonist into the periaqueductal gray upon electrically-induced vocalization in decerebrate cats. Neurosci Res 18:235–240PubMedCrossRef
go back to reference Schuller G, Radtke-Schuller S (1990) Neural control of vocalization in bats: mapping of brainstem areas with electrical microstimulation eliciting species-specific echolocation calls in the rufous horseshoe bat. Exp Brain Res 79:192–206CrossRefPubMed Schuller G, Radtke-Schuller S (1990) Neural control of vocalization in bats: mapping of brainstem areas with electrical microstimulation eliciting species-specific echolocation calls in the rufous horseshoe bat. Exp Brain Res 79:192–206CrossRefPubMed
go back to reference Schuller G, Fischer S, Schweizer H (1997) Significance of the paralemniscal tegmental area for audio-motor control in the mustached bat, Pteronotus parnellii: The afferent and efferent connections of the paralemniscal area. Eur J Neurosci 9:342–355PubMedCrossRef Schuller G, Fischer S, Schweizer H (1997) Significance of the paralemniscal tegmental area for audio-motor control in the mustached bat, Pteronotus parnellii: The afferent and efferent connections of the paralemniscal area. Eur J Neurosci 9:342–355PubMedCrossRef
go back to reference Sessle BJ, Ball GJ, Lucier GE (1981) Suppressive influences from periaqueductal gray and nucleus raphe magnus on respiration and related reflex activities and on solitary tract neurons, and effect of naloxone. Brain Res 216:145–161CrossRefPubMed Sessle BJ, Ball GJ, Lucier GE (1981) Suppressive influences from periaqueductal gray and nucleus raphe magnus on respiration and related reflex activities and on solitary tract neurons, and effect of naloxone. Brain Res 216:145–161CrossRefPubMed
go back to reference Shiba K, Umezaki T, Zheng Y, Miller AD (1997) The nucleus retroambigualis controls laryngeal muscle activity during vocalization in the cat. Exp Brain Res 115:513–519CrossRefPubMed Shiba K, Umezaki T, Zheng Y, Miller AD (1997) The nucleus retroambigualis controls laryngeal muscle activity during vocalization in the cat. Exp Brain Res 115:513–519CrossRefPubMed
go back to reference Siebert S, Jürgens U (2003) Vocalization after periaqueductal grey inactivation with the GABA agonist muscimol in the squirrel monkey. Neuroci Lett 340:111–114CrossRef Siebert S, Jürgens U (2003) Vocalization after periaqueductal grey inactivation with the GABA agonist muscimol in the squirrel monkey. Neuroci Lett 340:111–114CrossRef
go back to reference Thoms G, Jürgens U (1987) Common input of the cranial motor nuclei involved in phonation in squirrel monkey. Exp Neurol 95:85–99CrossRefPubMed Thoms G, Jürgens U (1987) Common input of the cranial motor nuclei involved in phonation in squirrel monkey. Exp Neurol 95:85–99CrossRefPubMed
go back to reference Todd NPM, Merker B (2004) Siamang gibbons exceed the saccular threshold: intensity of the song of Hylobates syndactilus. J Acoust Soc Am 115:3077–3080CrossRefPubMed Todd NPM, Merker B (2004) Siamang gibbons exceed the saccular threshold: intensity of the song of Hylobates syndactilus. J Acoust Soc Am 115:3077–3080CrossRefPubMed
go back to reference Ueyama T, Satoda T, Tashiro T, Sugimoto T, Matsushima R, Mizuno N (1990) Infrahyoid and accessory motoneurons in the Japanese monkey (Macaca fuscata). J Comp Neurol 291:373–382CrossRefPubMed Ueyama T, Satoda T, Tashiro T, Sugimoto T, Matsushima R, Mizuno N (1990) Infrahyoid and accessory motoneurons in the Japanese monkey (Macaca fuscata). J Comp Neurol 291:373–382CrossRefPubMed
go back to reference Veenman CL, Reiner A, Honig MG (1992) Biotinylated dextranamine as an anterograde tracer for single-labeling and double-labeling studies. J Neurosci Meth 41:239–254CrossRef Veenman CL, Reiner A, Honig MG (1992) Biotinylated dextranamine as an anterograde tracer for single-labeling and double-labeling studies. J Neurosci Meth 41:239–254CrossRef
go back to reference Winter P, Ploog D, Latta J (1966) Vocal repertoire of the squirrel monkey, its analysis and significance. Exp Brain Res 1:359–384CrossRefPubMed Winter P, Ploog D, Latta J (1966) Vocal repertoire of the squirrel monkey, its analysis and significance. Exp Brain Res 1:359–384CrossRefPubMed
go back to reference Zhang SP, Bandler R, Davis PJ (1995) Brain stem integration of vocalization: role of the nucleus retroambigualis. J Neurophysiol 74:2500–2512PubMed Zhang SP, Bandler R, Davis PJ (1995) Brain stem integration of vocalization: role of the nucleus retroambigualis. J Neurophysiol 74:2500–2512PubMed
go back to reference Zhang SP, Davis PJ, Carrive P, Bandler R (1992) Vocalization and marked pressor effect evoked from the region of the nucleus retroambigualis in the caudal ventrolateral medulla of the cat. Neurosci Lett 140:103–107CrossRefPubMed Zhang SP, Davis PJ, Carrive P, Bandler R (1992) Vocalization and marked pressor effect evoked from the region of the nucleus retroambigualis in the caudal ventrolateral medulla of the cat. Neurosci Lett 140:103–107CrossRefPubMed
Metadata
Title
Projections of the ventrolateral pontine vocalization area in the squirrel monkey
Authors
Stefanie Hannig
Uwe Jürgens
Publication date
01-02-2006
Publisher
Springer-Verlag
Published in
Experimental Brain Research / Issue 1/2006
Print ISSN: 0014-4819
Electronic ISSN: 1432-1106
DOI
https://doi.org/10.1007/s00221-005-0128-5

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