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Drinking: Hindbrain Sensorimotor Neural Organization

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Thirst

Part of the book series: ILSI Human Nutrition Reviews ((ILSI HUMAN))

Abstract

Numerous studies suggest that the patterned motor responses of drinking and swallowing are organized at the brainstem level (reviewed in Berntson and Micco 1976). Decerebration experiments further indicate that tactile and gustatory receptors can modify fluid intake using brainstem mechanisms, but that drinking to correct a water imbalance and spontaneous drinking both require an intact forebrain (Grill and Miselis 1981). Because only a fraction of an animal’s behaviour is evident when the forebrain and hindbrain are disconnected, decerebrate preparations provide an experimental method for establishing a gross anatomical location for function. Careful behavioural testing reveals those sensory and motor capacities that are intact, thereby allowing anatomical and physiological studies to be interpreted within the context of a limited, but specific, behavioural repertoire. The first section of this chapter reviews the sensorimotor capacity of the decerebrate preparation with respect to ingestive behaviour. This is followed by several sections discussing brainstem pathways mediating these responses.

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References

  • 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 283:248–268

    Article  PubMed  CAS  Google Scholar 

  • Amano N, Hu JW, Sessle BJ (1986) Responses of neurons in feline trigeminal subnucleus caudalis (medullary dorsal horn) to cutaneous, intraoral, and muscle afferent stimuli. J Neurophysiol 55:227–243

    PubMed  CAS  Google Scholar 

  • Amri M, Car A (1988) Projections from the medullary swallowing center to the hypoglossal motor nucleus: a neuroanatomical and electrophysiological study in sheep. Brain Res 441:119–126

    Article  PubMed  CAS  Google Scholar 

  • Amri M, Car A, Jean A (1984) Medullary control of the pontine swallowing neurones in sheep. Exp Brain Res 55:105–110

    Article  PubMed  CAS  Google Scholar 

  • Beckstead RM, Domesick VB, Nauta WJH (1979) Efferent connections of the substantia nigra and ventral tegmental area in the rat. Brain Res 175:191–217

    Article  PubMed  CAS  Google Scholar 

  • Berntson GG, Micco DJ (1976) Organization of brainstem behavioral systems. Brain Res Bull 1:471–483

    Article  PubMed  CAS  Google Scholar 

  • Bieger D (1984) Muscarinic activation of rhombencephalic neurones controlling oesophageal peristalsis in the rat. Neuropharmacology 23:1451–1464

    Article  PubMed  CAS  Google Scholar 

  • Bignall KE, Schramm L (1974) Behavior of chronically decerebrated kittens. Exp Neurol 42:519–531

    Article  PubMed  CAS  Google Scholar 

  • Borke RC, Nau ME, Ringler RL Jr (1983) Brain stem afferents of hypoglossal neurons in the rat. Brain Res 269:47–55

    Article  PubMed  CAS  Google Scholar 

  • Car A, Amri M (1982) Etude des neurones deglutiteurs pontiques chez la brebis: I. Activite et localisation. Exp Brain Res 48:345–354

    Article  PubMed  CAS  Google Scholar 

  • Car A, Amri M (1987) Activity of neurons located in the region of the hypoglossal motor nucleus during swallowing in sheep. Exp Brain Res 69:175–182

    Article  PubMed  CAS  Google Scholar 

  • Carrive P, Bandler R, Dampney RAL (1989) Viscerotopic control of regional vascular beds by discrete groups of neurons within the midbrain periaqueductal gray. Brain Res 493:385–390

    Article  PubMed  CAS  Google Scholar 

  • Chandler SH, Goldberg LJ (1984) Differentiation of the neural pathways mediating cortically induced and dopaminergic activation of the central pattern generator (CPG) for rhythmical jaw movements in the anesthetized guinea pig. Brain Res 323:297–301

    Article  PubMed  CAS  Google Scholar 

  • Chandler SH, Tal M (1986) The effects of brain stem transections on the neuronal networks responsible for rhythmical jaw muscle activity in the guinea pig. J Neurosci 6:1831–1842

    PubMed  CAS  Google Scholar 

  • Chandler SH, Tal M (1987) Brain-stem perturbations during cortically evoked rhythmical jaw movements: effects of activation of brain-stem loci on jaw muscle cycle characteristics. J Neurosci 7:463–472

    PubMed  CAS  Google Scholar 

  • Chronister RB, Walding JS, Aides LD, Marco LA (1988) Interconnections between substantia nigra reticulata and medullary reticular formation. Brain Res Bull 21:313–317

    Article  PubMed  CAS  Google Scholar 

  • Dellow PG, Lund JP (1971) Evidence for central timing of rhythmical mastication. J Physiol 215:1–13

    PubMed  CAS  Google Scholar 

  • Dostrovsky JO, Hu JW, Sessle BJ, Sumino R. (1982) Stimulation sites in periaqueductal gray, nucleus raphe magnus and adjacent regions effective in suppressing oral-facial reflexes. Brain Res 252:287–297

    Article  PubMed  CAS  Google Scholar 

  • Ermirio R, Guggeri P, Blanchi D, Cogo CE, Bergaglio M (1989) Effects of intraoral mechanoreceptor stimulation on reticular formation neurones in the rabbit. Arch Ital Biol 127:1–11

    PubMed  CAS  Google Scholar 

  • Gerstner GE, Goldberg LJ, De Bruyne K (1989) Angiotensin Il-induced rhythmic jaw movements in the ketamine-anesthetized guinea pig. Brain Res 478:233–240

    Article  PubMed  CAS  Google Scholar 

  • Grill HJ (1986) Caudal brainstem contributions to the integrated neural control of energy homeostasis. In: Ritter RC (ed) Feeding behavior: neural and hormonal controls. Academic Press, New York, pp 103–129

    Google Scholar 

  • Grill HJ, Miselis RR (1981) Lack of ingestive compensation to osmotic stimuli in chronic decerebrate rats. Am J Physiol 240:81–86

    Google Scholar 

  • Grill HJ, Norgren R (1978) Chronically decerebrate rats demonstrate satiation but not bait shyness. Science 201:267–269

    Article  PubMed  CAS  Google Scholar 

  • Grill HJ, Schulkin J, Flynn FW (1986) Sodium homeostasis in chronic decerebrate rats. Behav Neurosci 100:536–543

    Article  PubMed  CAS  Google Scholar 

  • Hashim MA, Bieger D (1989) Excitatory amino acid receptor-mediated activation of solitarial deglutitive loci. Neuropharmacology 28:913–921

    Article  PubMed  CAS  Google Scholar 

  • Hayama T, Ito S, Ogawa H (1987) Receptive field properties of the parabrachio-thalamic taste and mechanoceptive neurons in rats. Exp Brain Res 68:458–465

    Article  PubMed  CAS  Google Scholar 

  • Hermann GE, Rogers RC (1985) Convergence of vagal and gustatory afferent input within the parabrachial nucleus of the rat. J Auton Nerv Syst 13:1–17

    Article  PubMed  CAS  Google Scholar 

  • Hiraba K, Taira M, Sahara Y, Nakamura Y (1988) Single-unit activity in bulbar reticular formation during food ingestion in chronic cats. J Neurophysiol 60:1333–1349

    PubMed  CAS  Google Scholar 

  • Holstege G (1987) Some anatomical observations on the projections from the hypothalamus to brainstem and spinal cord: an HRP and autoradiographic tracing study in the cat. J Comp Neurol 260:98–126

    Article  PubMed  CAS  Google Scholar 

  • Jean A (1984) Control of the central swallowing program by inputs from the peripheral receptors. A review. J Auton Nerv Syst 10:225–233

    Article  PubMed  CAS  Google Scholar 

  • Jean A, Car A, Roman C (1975) Comparison of activity in pontine versus medullary neurones during swallowing. Exp Brain Res 22:211–220

    Article  PubMed  CAS  Google Scholar 

  • Joseph JP, Boussaoud D, Biguer B (1985) Activity of neurons in the cat substantia nigra pars reticulata during drinking. Exp Brain Res 60:375–379

    Article  PubMed  CAS  Google Scholar 

  • Junquera J, Lanzagorta-Sanchez G, Mejia-Perez BE, Racotta R (1984) Motor activity in decerebrate rats: spontaneous and nutrient-induced changes. Am J Physiol 247:R945–R952

    PubMed  CAS  Google Scholar 

  • Kessler JP, Jean A (1985) Identification of the medullary swallowing regions in the rat. Exp Brain Res 57:256–263

    Article  PubMed  CAS  Google Scholar 

  • Kornblith CL, Hall WG (1979) Brain transections selectively alter ingestion and behavioral activation in neonatal rats. J Comp Physiol Psychol 93:1109–1117

    Article  PubMed  CAS  Google Scholar 

  • Kruger L, Michel F (1962) A single neuron analysis of buccal cavity representation in the sensory trigeminal complex of the cat. Arch Oral Biol 7:491–503

    Article  PubMed  CAS  Google Scholar 

  • Kucharczyk J, Mogenson GJ (1975) Separate lateral hypothalamic pathways for extracellular and intracellular thirst. Am J Physiol 228:295–301

    PubMed  CAS  Google Scholar 

  • Lovick TA (1972) The behavioural repertoire of precollicular decerebrate rats. J Physiol (Lond) 226:4P–6P

    CAS  Google Scholar 

  • Lund JP (1984) Sensorimotor integration in the control of mastication. In: Klienberg I, Sessle B (eds) Oro-facial pain and neuromuscular dysfunction: mechanisms and clinical correlates, vol 52. Advances in biosciences. Pergamon Press, Oxford, pp 51–65

    Google Scholar 

  • Luschei ES (1987) Central projections of the mesencephalic nucleus of the fifth nerve: an autoradiographic study. J Comp Neurol 263:137–145

    Article  PubMed  CAS  Google Scholar 

  • Malmo RB (1976) Osmosensitive neurons in the rat’s dorsal midbrain. Brain Res 105:105–120

    Article  PubMed  CAS  Google Scholar 

  • Mark GP, Scott TR, Chang F-C T, Grill HJ (1988) Taste responses in the nucleus tractus solitarius of the chronic decerebrate rat. Brain Res 443:137–148

    Article  PubMed  CAS  Google Scholar 

  • Mason P, Strassman A, Maciewicz R (1985) Is the jaw-opening reflex a valid model of pain. Brain Res Rev 10:137–146

    Article  Google Scholar 

  • McNamara JA Jr, Moyers RE (1973) Electromyography of the oral phase of deglutition in the rhesus monkey (Macaca mulatta). Arch Oral Biol 18:995–1002

    Article  Google Scholar 

  • Miller AJ (1982) Deglutition. Physiol Rev 62:129–184

    PubMed  CAS  Google Scholar 

  • Moriyama Y (1987) Rhythmical jaw movements and lateral pontomedullary reticular neurons in rats. Comp Biochem Physiol 86A:7–14

    Article  Google Scholar 

  • Nakamura Y, Kubo Y (1978) Masticatory rhythm in intracellular potential of trigeminal motoneurons induced by stimulation of orbital cortex and amygdala in cats. Brain Res 148:504–509

    Article  PubMed  CAS  Google Scholar 

  • Norgren R (1978) Projections from the nucleus of the solitary tract in the rat. Neuroscience 3:207–218

    Article  PubMed  CAS  Google Scholar 

  • Norgren R (1985) Taste and the autonomic nervous system. Chem Senses 10:143–161

    Article  Google Scholar 

  • Norgren R, Leonard CM (1973) Ascending central gustatory pathways. J Comp Neurol 150:217–238

    Article  PubMed  CAS  Google Scholar 

  • Nozaki S, Enomoto S, Nakamura Y (1983) Identification and input-output properties of bulbar reticular neurons involved in the cerebral cortical control of trigeminal motoneurons in cats. Exp Brain Res 49:363–372

    Article  PubMed  CAS  Google Scholar 

  • Nozaki S, Iriki A, Nakamura Y (1986a) Localization of central rhythm generator involved in cortically induced rhythmical masticatory jaw-opening movement in the guinea pig. J Neurophysiol 55:806–825

    PubMed  CAS  Google Scholar 

  • Nozaki S, Iriki A, Nakamura Y (1986b) Role of corticobulbar projection neurons in cortically induced rhythmical masticatory jaw-opening in the guinea pig. J Neurophysiol 55:826–845

    PubMed  CAS  Google Scholar 

  • Ogawa H, Hayama T, Yamashita Y (1988) Thermal sensitivity of neurons in a rostral part of the rat solitary tract nucleus. Brain Res 454:321–331

    Article  PubMed  CAS  Google Scholar 

  • Olsson KA, Sasamoto K, Lund JP (1986) Modulation of transmission in rostral trigeminal sensory nuclei during chewing. J Neurophysiol 55:56–75

    PubMed  CAS  Google Scholar 

  • Saper CB, Loewy AD (1980) Efferent connections of the parabrachial nucleus in the rat. Brain Res 197:291–317

    Article  PubMed  CAS  Google Scholar 

  • Scheibel ME, Scheibel AB (1958) Structural substrates for integrative patterns in the brain stem reticular core. In: Jasper HH et al. (eds) Reticular formation of the brain. Little Brown, Boston, pp 31–55

    Google Scholar 

  • Schneider JS (1986) Interactions between the basal ganglia, the pontine parabrachial region, and the trigeminal system in cats. Neuroscience 19:411–425

    Article  PubMed  CAS  Google Scholar 

  • Schneider JS, Manettto C, Lidsky TI (1985) Substantia nigra projection to medullary reticular formation: relevance to oculomotor and related motor functions in the cat. Neurosci Lett 62:1–6

    Article  PubMed  CAS  Google Scholar 

  • Scott TR, Yaxley S, Sienkiewicz ZJ, Rolls ET (1986) Gustatory responses in the nucleus tractus solitarius of the alert cynomologous monkey. J Neurophysiol 55:182–200

    PubMed  CAS  Google Scholar 

  • Sessle BJ, Greenwood LF (1976) Inputs to trigeminal brain stem neurons from facial, oral, tooth pulp and pharyngolaryngeal tissues: I responses to innocuous and noxious stimuli. Brain Res 117:211–226

    Article  PubMed  CAS  Google Scholar 

  • Steiner JE (1973) The gustofacial response: observation on normal and anencephalic newborn infants. In: Bosma JF (ed) Oral sensation and perception: development in the fetus and infant. US Department of Health, Education and Welfare, Bethesda, pp 254–278

    Google Scholar 

  • Storey AT (1968) A functional analysis of sensory units innervating epiglottis and larynx. Exp Neurol 20:366–383

    Article  PubMed  CAS  Google Scholar 

  • Sumi T (1970) Activity in single hypoglossal fibers during cortically induced swallowing and chewing in rabbits. Pflügers Arch 314:329–346

    Article  PubMed  CAS  Google Scholar 

  • Suzuki SS, Siegel JM (1985) Reticular formation neurons related to tongue movement in the behaving cat. Exp Neurol 89:689–697

    Article  PubMed  CAS  Google Scholar 

  • Swanson LW, Sharpe LG (1973) Centrally induced drinking: comparison of angiotensin II- and carbachol-sensitive sites in rats. Am J Physiol 225:566–573

    PubMed  CAS  Google Scholar 

  • Swanson LW, Kucharczyk J, Mogenson GJ (1978) Autoradiographic evidence for pathways from the medial preoptic area to the midbrain involved in the drinking response to angiotensin II. J Comp Neurol 178:645–660

    Article  PubMed  CAS  Google Scholar 

  • Sweazey RD, Bradley RM (1987) Responses of lamb spinal trigeminal nucleus neurons to mechanical, thermal and chemical stimulations of the oral cavity and epiglottis. Soc Neurosci Abstr p 779

    Google Scholar 

  • Sweazey RD, Bradley RM (1988) Responses of lamb nucleus of the solitary tract neurons to chemical stimulation of the epiglottis. Brain Res 439:195–210

    Article  PubMed  CAS  Google Scholar 

  • Sweazey RD, Bradley RM (1989) Responses of neurons in the lamb nucleus tractus solitarius to stimulation of the caudal oral cavity and epiglottis with different stimulus modalities. Brain Res 480:133–150

    Article  PubMed  CAS  Google Scholar 

  • Tal M (1987) Neural basis for initiation of rhythmic digastric activity upon midbrain stimulation in the guinea pig. Brain Res 411:58–64

    Article  PubMed  CAS  Google Scholar 

  • Thexton AJ, Crompton AW (1989) Effect of sensory input from the tongue on jaw movement in normal feeding opossum. J Exp Zool 250:233–243

    Article  PubMed  CAS  Google Scholar 

  • Thexton AJ, Griffiths C (1979) Reflex oral activity in decerebrate rats of different age. Brain Res 175:1–9

    Article  PubMed  CAS  Google Scholar 

  • Thexton AJ, McGarrick J (1987) Effect of experimentally elicited rhythmic oral activity on the linguodigastric reflex in the lightly anesthetized rabbit. Exp Neurol 96:104–117

    Article  PubMed  CAS  Google Scholar 

  • Travers JB (1988) Efferent projections from the anterior nucleus of the solitary tract of the hamster. Brain Res 457:1–11

    Article  PubMed  CAS  Google Scholar 

  • Travers JB (1989) Hypoglossal unit activity during licking and swallowing. J Dent Res 68:309

    Google Scholar 

  • Travers JB, Jackson LM (1989) The effects of gustatory stimulation on neurons in and adjacent to the hypoglossal nucleus. Chem Senses 14:756

    Article  Google Scholar 

  • Travers JB, Norgren R (1983) Afferent projections to the oral motor nuclei in the rat. J Comp Neurol 220:280–298

    Article  PubMed  CAS  Google Scholar 

  • Travers JB, Norgren R (1986) Electromyographic analysis of the ingestion and rejection of sapid stimuli in the rat. Behav Neurosci 100:544–555

    Article  PubMed  CAS  Google Scholar 

  • Travers SP, Norgren R (1988) Oral sensory responses in the nucleus of the solitary tract. Soc Neurosci Abstr p 1185

    Google Scholar 

  • Travers SP, Pfaffmann C, Norgren R (1986) Convergence of lingual and palatal gustatory neural activity in the nucleus of the solitary tract. Brain Res 365:305–320

    Article  PubMed  CAS  Google Scholar 

  • Travers JB, Waltzer R, Travers S (1988) Sensory-motor mapping of the solitary nucleus and adjacent structures. Chem Senses 13:741

    Google Scholar 

  • Van Willigen JD, Weijs-Boot J (1984) Phasic and rhythmic responses of the oral musculature to mechanical stimulation of the rat palate. Arch Oral Biol 29:7–11

    Article  PubMed  Google Scholar 

  • White NM (1986) Control of sensorimotor functions by dopaminergic nigrostriatal neurons: influence on eating and drinking. Neurosci Biobehav Rev 10:15–36

    Article  PubMed  CAS  Google Scholar 

  • Whitehead MC (1988) Neuronal architecture of the nucleus of the solitary tract in the hamster. J Comp Neurol 276:547–572

    Article  PubMed  CAS  Google Scholar 

  • Whitehead MC, Savoy LD (1987) The solitary nucleus of the hamster. Ann N Y Acad Sci 510:707–709

    Article  Google Scholar 

  • Woods, JW (1964) Behavior of chronic decerebrate rats. J Neurophysiol 27:635–644

    PubMed  CAS  Google Scholar 

  • Zeigler HP, Jacquin MF, Miller MG (1985) Trigeminal orosensation and ingestive behavior in the rat. Prog Psychobiol Physiol Psychol 11:63–195

    Google Scholar 

  • Zhang G, Sasamoto K (1990) Projections of two separate cortical areas for rhythmical jaw movements in the rat. Brain Res Bull 24:221–230

    Article  PubMed  CAS  Google Scholar 

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  1. J. B. Travers
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Editors and Affiliations

  1. University of California - San Francisco, 94103-0400, San Francisco, CA, USA

    David J. Ramsay MA,DM,DPhil (Professor of Physiology and Senior Vice Chancellor) (Professor of Physiology and Senior Vice Chancellor)

  2. Nutritional Psychology Research Group, School of Psychology, University of Birmingham, B15 2TT, Edgbaston, Birmingham, UK

    David Booth MA,BSc,BA,PhD,DSc,CPsychol,FBPsS (Professor of Psychology) (Professor of Psychology)

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© 1991 Springer-Verlag London Limited

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Travers, J.B. (1991). Drinking: Hindbrain Sensorimotor Neural Organization. In: Ramsay, D.J., Booth, D. (eds) Thirst. ILSI Human Nutrition Reviews. Springer, London. https://doi.org/10.1007/978-1-4471-1817-6_16

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  • DOI: https://doi.org/10.1007/978-1-4471-1817-6_16

  • Publisher Name: Springer, London

  • Print ISBN: 978-1-4471-1819-0

  • Online ISBN: 978-1-4471-1817-6

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