Skip to main content

Advertisement

Log in

Parabrachial nucleus neuronal responses to off-vertical axis rotation in macaques

  • Research Article
  • Published:
Experimental Brain Research Aims and scope Submit manuscript

Abstract

The caudal aspect of the parabrachial nucleus (PBN) contains neurons responsive to whole body, periodic rotational stimulation in alert monkeys (Balaban et al. in J Neurophysiol 88:3175–3193, 2002). This study characterizes the angular and linear motion-sensitive response properties of PBN unit responses during off-vertical axis rotation (OVAR) and position trapezoid stimulation. The OVAR responses displayed a constant firing component which varied from the firing rate at rest. Nearly two-thirds of the units also modulated their discharges with respect to head orientation (re: gravity) during constant velocity OVAR stimulation. The modulated response magnitudes were equal during ipsilateral and contralateral OVARs, indicative of a one-dimensional accelerometer. These response orientations during OVAR divided the units into three spatially tuned populations, with peak modulation responses centered in the ipsilateral ear down, contralateral anterior semicircular canal down, and occiput down orientations. Because the orientation of the OVAR modulation response was opposite in polarity to the orientation of the static tilt component of responses to position trapezoids for the majority of units, the linear acceleration responses were divided into colinear dynamic linear and static tilt components. The orientations of these unit responses formed two distinct population response axes: (1) units with an interaural linear response axis and (2) units with an ipsilateral anterior semicircular canal-contralateral posterior semicircular canal plane linear response axis. The angular rotation sensitivity of these units is in a head-vertical plane that either contains the linear acceleration response axis or is perpendicular to the linear acceleration axis. Hence, these units behave like head-based (‘strapdown’) inertial guidance sensors. Because the PBN contributes to sensory and interoceptive processing, it is suggested that vestibulo-recipient caudal PBN units may detect potentially dangerous anomalies in control of postural stability during locomotion. In particular, these signals may contribute to the range of affective and emotional responses that include panic associated with falling, malaise associated with motion sickness and mal-de-debarquement, and comorbid balance and anxiety disorders.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10

Similar content being viewed by others

References

  • Angelaki DE, Dickman JD (2000) Spatiotemporal processing of linear acceleration: primary afferent and central vestibular neuron responses. J Neurophysiol 84:2113–2132

    CAS  PubMed  Google Scholar 

  • Balaban CD (1996) Vestibular nucleus projections to the parabrachial nucleus in rabbits: implications for vestibular influences on autonomic function. Exp Brain Res 108:367–381

    Article  CAS  PubMed  Google Scholar 

  • Balaban CD (1999) Vestibular autonomic regulation. Curr Opin Neurol 12:29–33

    Article  CAS  PubMed  Google Scholar 

  • Balaban CD (2004) Projections from the parabrachial nucleus to the vestibular nuclei: potential substrates for autonomic and limbic influences on vestibular responses. Brain Res 996:126–137

    Article  CAS  PubMed  Google Scholar 

  • Balaban CD, Thayer JF (2001) Neurological bases for balance-anxiety links. J Anxiety Disord 15:53–79

    Article  CAS  PubMed  Google Scholar 

  • Balaban CD et al (2002) Responses of primate caudal parabrachial nucleus and Kölliker-Fuse nucleus neurons to whole body rotation. J Neurophysiol 88:3175–3193

    Article  PubMed  Google Scholar 

  • Bernard JF (1996) Involvement of the spino-parabrachio-amygdaloid and -hypothalmic systems in the autonomic and emotional aspects of pain. In: Hostege G et al (eds) The emotional motor system, vol 107. Elsevier, Amsterdam, pp 243–255

    Chapter  Google Scholar 

  • Bernard JF, Besson J-M (1990) The spino (trigemino) pontoamygdaloid pathway: electrophysiological evidence for an involvement in pain processes. J Neurophysiol 63:473–490

    CAS  PubMed  Google Scholar 

  • Bernard J-F et al (1993) The organization of the efferent projections from the pontine parabrachial area to the amygdaloid complex: a Phaselus vulgaris leucoagglutinin (PHA-L) study in the rat. J Comp Neurol 329:201–229

    Article  CAS  PubMed  Google Scholar 

  • Bester H et al (1995) Spino (trigemino) parabrachiohypothalamic pathway: electrophysiological evidence for an involvement in pain processes. J Neurophysiol 73:568–585

    CAS  PubMed  Google Scholar 

  • Bester H et al (2000) Physiological properties of the lamina I spinoparabrachial neurons in the rat. J Neurophysiol 83:2239–2259

    CAS  PubMed  Google Scholar 

  • Bezdek JC (1981) Pattern recognition with fuzzy objective function algorithms. Plenum, New York

    Google Scholar 

  • Cameron OG (2002) Visceral sensory neuroscience. Oxford University Press, New York

    Google Scholar 

  • Chamberlin NL, Saper CB (1992) Topographic organization of cardiovascular responses to electrical and glutamate microstimulation of the parabrachial nucleus in the rat. J Comp Neurol 326:245–262

    Article  CAS  PubMed  Google Scholar 

  • Chamberlin NL, Saper CB (1994) Topographic organization of respiratory responses to glutamate microstimulation of the parabrachial nucleus in the rat. J Neurosci 14:6500–6510

    CAS  PubMed  Google Scholar 

  • Collewijn H (1977) Eye- and head movements in freely moving rabbits. J Physiol 266:471–498

    CAS  PubMed  Google Scholar 

  • Craig AD (2002) How do you feel? Interoception: the sense of the physiological condition of the body. Nat Rev Neurosci 3:655–666

    CAS  PubMed  Google Scholar 

  • Craig AD (2003) A new view of pain as a homeostatic emotion. Trends Neurosci 26:303–307

    Article  CAS  PubMed  Google Scholar 

  • Craig AD (2009) How do you feel–now? The anterior insula and human awareness. Nat Rev Neurosci 10:59–70

    Article  CAS  PubMed  Google Scholar 

  • David HA (1970) Order statistics. Wiley, New York

    Google Scholar 

  • Dickman JD, Angelaki DE (2002) Vestibular convergence patterns in vestibular nuclei neurons of alert primates. J Neurophysiol 88:3518–3533

    Article  PubMed  Google Scholar 

  • Dunbar DC, Badam GL (1998) Development of posture and locomotion in free-ranging primates. Neurosci Biobehav Rev 22:541–546

    Article  CAS  PubMed  Google Scholar 

  • Dunbar DC et al (2004) Stabilization and mobility of the head and trunk in wild monkeys during terrestrial and flat-surface walks and gallops. J Exp Biol 207:1027–1042

    Article  PubMed  Google Scholar 

  • Fanselow MS (1994) Neural organization of the defensive behavior system responsible for fear. Psychon Bull Rev 1:429–438

    Google Scholar 

  • Feil K, Herbert H (1995) Topographic organization of spinal and trigeminal somatosensory pathways to the rat parabrachial and Kölliker-Fuse nuclei. J Comp Neurol 353:506–528

    Article  CAS  PubMed  Google Scholar 

  • Fulweiler CE, Saper C (1984) Subnuclear organization of the efferent connections of the parabrachial nucleus in the rat. Brain Res Rev 7:229–259

    Article  Google Scholar 

  • Gauriau C, Bernard J-F (2002) Pain pathways and parabrachial circuits in the rat. Exp Physiol 87:251–258

    Article  PubMed  Google Scholar 

  • Graybiel A, Knepton J (1976) Sopite syndrome: a sometimes sole manifestation of motion sickness. Aviat Space Environ Med 47:873–882

    CAS  PubMed  Google Scholar 

  • Grigson PS et al (1998a) The parabrachial nucleus is essential for acquisition of a conditioned odor aversion in rats. Behav Neurosci 112:1104–1113

    Article  CAS  PubMed  Google Scholar 

  • Grigson PS et al (1998b) Ibotenic acid lesions of the parabrachial nucleus and conditioned taste aversion: further evidence for an associative deficit in rats. Behav Neurosci 112:160–171

    Article  CAS  PubMed  Google Scholar 

  • Grossman GE et al (1988) Frequency and velocity of rotational head perturbations during locomotion. Exp Brain Res 70:470–476

    Article  CAS  PubMed  Google Scholar 

  • Hade JS et al (1988) Stimulation of parabrachial neurons elicits a sympathetically mediated pressor response in cats. Am J Physiol 255:H1349–H1358

    CAS  PubMed  Google Scholar 

  • Hayward LF, Felder RB (1998) Lateral parabrachial nucleus modulates baroreflex regulation of sympathetic nerve activity. Am J Physiol 274:R1274–R1282

    CAS  PubMed  Google Scholar 

  • Herbert H et al (1990) Connections of the parabrachial nucleus with the nucleus of the solitary tract and medullary reticular formation in the rat. J Comp Neurol 293:540–580

    Article  CAS  PubMed  Google Scholar 

  • Jasmin L et al (1997) Transneuronal labeling of a nociceptive pathway, the spino-(trigemino-)parabrachio-amygdaloid, in the rat. J Neurosci 17:3751–3765

    CAS  PubMed  Google Scholar 

  • Jhamandas JH et al (1991) Cardiovascular influences on rat parabrachial nucleus: an electrophysiological study. Am J Physiol 260:R225–R231

    CAS  PubMed  Google Scholar 

  • Kasper J et al (1988) Response of vestibular neurons to head rotations in vertical planes. I. Response to vertical stimulation. J Neurophysiol 60:1753–1760

    CAS  PubMed  Google Scholar 

  • Ma W, Peschanski M (1988) Spinal and trigeminal projections to the parabrachial nucleus in the rat: electron-microscopic evidence of a spino-ponto-amygdalian somatosensory pathway. Somatosens Res 5:247–257

    Article  CAS  PubMed  Google Scholar 

  • Mardia KV, Jupp PE (2000) Directional statistics, vol. Wiley, Chichester

    Google Scholar 

  • Mayer T et al (1993) Noninvasive measurement of cervical tri-planar motion in normal subjects. Spine 18:2191–2195

    Article  CAS  PubMed  Google Scholar 

  • Mayo H (1837) Outlines of human physiology. Henry Renshaw and J. Churchill, London

    Google Scholar 

  • Moga MM et al (1990) Organization of cortical, basal forebrain, and hypothalamic afferents to the parabrachial nucleus in the rat. J Comp Neurol 295:624–661

    Article  CAS  PubMed  Google Scholar 

  • Money KE (1970) Motion sickness. Physiol Rev 50:1–39

    CAS  PubMed  Google Scholar 

  • Money KE (1996) The autonomic nervous system and motion sickness. In: Yates BJ, Miller AD et al (eds) Vestibular autonomic regulation. CRC Press, Boca Raton, pp 147–173

    Google Scholar 

  • Mulavara AP et al (2002) Modulation of head movement control in humans during treadmill walking. Gait Posture 16:271–282

    Article  PubMed  Google Scholar 

  • Musallam S, Tomlinson RD (2002) Asymmetric integration recorded from vestibular-only cells in response to position transients. J Neurophysiol 88:2104–2113

    PubMed  Google Scholar 

  • Nishijo H, Norgren R (1997) Parabrachial neural coding of taste stimuli in awake rats. J Neurophysiol 78:2254–2268

    CAS  PubMed  Google Scholar 

  • Norgren R (1976) Taste pathways to hypothalamus and amygdala. J Comp Neurol 166:17–30

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Norgren R, Pfaffmann C (1975) The pontine taste area in the rat. Brain Res 91:99–117

    Article  CAS  PubMed  Google Scholar 

  • Porter JD, Balaban CD (1997) Connections between the vestibular nuclei and regions that mediate autonomic function in the rat. J Vestib Res 7:63–76

    Article  CAS  PubMed  Google Scholar 

  • Pozzo T et al (1990) Head stabilization during various locomotor tasks in humans. Exp Brain Res 82:97–102

    Article  CAS  PubMed  Google Scholar 

  • Pozzo T et al (1995) Head and trunk movements in the frontal plane during complex dynamic equilibrium tasks in humans. Exp Brain Res 106:327–338

    Article  CAS  PubMed  Google Scholar 

  • Pritchard TC et al (2000) Projections of the parabrachial nucleus in the Old World monkey. Exp Neurol 165:101–117

    Article  CAS  PubMed  Google Scholar 

  • Reason JT, Brand JJ (1975) Motion sickness. Academic Press, London

    Google Scholar 

  • Reilly S, Trufinovic R (2000) Lateral parabrachial nucleus lesions in the rat: aversive and appetitive gustatory conditioning. Brain Res Bull 52:269–278

    Article  CAS  PubMed  Google Scholar 

  • Reilly S, Trifunovic R (2001) Lateral parabrachial nucleus lesions in the rat: neophobia and conditioned taste aversion. Brain Res Bull 55:359–366

    Article  CAS  PubMed  Google Scholar 

  • Reisine H, Raphan T (1992) Neural basis for eye velocity generation in the vestibular nuclei of alert monkeys during off-vertical axis stimulation. Exp Brain Res 92:209–226

    Article  CAS  PubMed  Google Scholar 

  • Saleh TM, Connell BJ (1998) The parabrachial nucleus mediates the decreased cardiac baroreflex sensitivity observed following short-term visceral afferent activation. Neuroscience 87:135–146

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Schor RH et al (1984) Responses to head tilt in cat central vestibular neurons. I. Direction of maximum sensitivity. J Neurophysiol 51:136–146

    CAS  PubMed  Google Scholar 

  • Schor RH et al (1985) Responses to head tilt in cat central vestibular neurons. II. Frequency dependence of neural response vectors. J Neurophysiol 53:1444–1452

    CAS  PubMed  Google Scholar 

  • Schroer RB (1984) From autopilot to strapdown: electrotechnology in inertial guidance and control. IEEE Trans Aerosp Electron Syst AES-20 pp 445–454

  • Shimura T et al (1997) Salient responsiveness of parabrachial neurons to the conditioned stimulus after the acquisition of taste aversion learning in rats. Neuroscience 81:239–247

    Article  CAS  PubMed  Google Scholar 

  • Shumway RH, Stoffer DS (2006) Time series analysis and its applications: with R examples. Springer Science-Business Media LLC, New York

    Google Scholar 

  • Song G et al (2006) Cytoarchitecture of pneumotaxic integration of respiratory and non respiratory information in the rat. J Neurosci 26:300–310

    Article  CAS  PubMed  Google Scholar 

  • Spector AC et al (1992) Parabrachial gustatory lesions impair taste aversion learning in rats. Behav Neurosci 106:147–161

    Article  CAS  PubMed  Google Scholar 

  • Tyler DB, Bard P (1949) Motion sickness. Physiol Rev 29:311–369

    CAS  PubMed  Google Scholar 

  • Wilson VJ et al (1986) Spatial organization of neck and vestibular reflexes acting on the forelimbs of the decerebrate cat. J Neurophysiol 55:514–526

    Google Scholar 

  • Yamamoto T et al (1995) Conditioned taste aversion in rats with excitotoxic brain lesions. Neurosci Res 22:31–49

    Article  CAS  PubMed  Google Scholar 

  • Yasui Y et al (1985) Direct cortical projections to the parabrachial nucleus in the cat. J Comp Neurol 234:77–86

    Article  CAS  PubMed  Google Scholar 

  • Yoshida A et al (1997) Organization of the descending projections from the parabrachial nucleus to the trigeminal sensory nuclear complex and the spinal dorsal horn in the rat. J Comp Neurol 383:94–111

    Article  CAS  PubMed  Google Scholar 

  • Zhou W et al (2006) Responses of monkey vestibular-only neurons to translation and angular rotation. J Neurophysiol 96:2915–2930

    Article  PubMed  Google Scholar 

  • Zylka M (2005) Nonpeptidergic circuits feel your pain. Neuron 47:771–772

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This research was supported by the National Institutes of Health (United States of America), grant nos R01 DC000739 (C.D.B.) and F31 DC006321 (C.H.M). The authors gratefully acknowledge valuable collegial advice from Dr. Robert H. Schor and expert histological assistance from Gloria Limetti and Jeanne Betsch.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Carey D. Balaban.

Rights and permissions

Reprints and permissions

About this article

Cite this article

McCandless, C.H., Balaban, C.D. Parabrachial nucleus neuronal responses to off-vertical axis rotation in macaques. Exp Brain Res 202, 271–290 (2010). https://doi.org/10.1007/s00221-009-2130-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00221-009-2130-9

Keywords

Navigation