Skip to main content

Advertisement

Log in

Neurochemical organization of the vestibular brainstem in the common chimpanzee (Pan troglodytes)

Brain Structure and Function Aims and scope Submit manuscript

Abstract

Chimpanzees are one of the closest living relatives of humans. However, the cognitive and motor abilities of chimpanzees and humans are quite different. The fact that humans are habitually bipedal and chimpanzees are not implies different uses of vestibular information in the control of posture and balance. Furthermore, bipedal locomotion permits the development of fine motor skills of the hand and tool use in humans, suggesting differences between species in the structures and circuitry for manual control. Much motor behavior is mediated via cerebro-cerebellar circuits that depend on brainstem relays. In this study, we investigated the organization of the vestibular brainstem in chimpanzees to gain insight into whether these structures differ in their anatomy from humans. We identified the four nuclei of vestibular nuclear complex in the chimpanzee and also looked at several other precerebellar structures. The size and arrangement of some of these nuclei differed between chimpanzees and humans, and also displayed considerable inter-individual variation. We identified regions within the cytoarchitectonically defined medial vestibular nucleus visualized by immunoreactivity to the calcium-binding proteins calretinin and calbindin as previously shown in other species including human. We have found that the nucleus paramedianus dorsalis, which is identified in the human but not in macaque monkeys, is present in the chimpanzee brainstem. However, the arcuate nucleus, which is present in humans, was not found in chimpanzees. The present study reveals major differences in the organization of the vestibular brainstem among Old World anthropoid primate species. Furthermore, in chimpanzees, as well as humans, there is individual variability in the organization of brainstem nuclei.

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
Fig. 11
Fig. 12
Fig. 13
Fig. 14
Fig. 15
Fig. 16
Fig. 17
Fig. 18

Abbreviations

Arc:

Arcuate nucleus

CB:

Calbindin

CR:

Calretinin

CV:

Cresyl violet

DCN:

Dorsal cochlear nucleus

DE:

Dentate nucleus

ECu:

External (lateral) cuneate nucleus

EF:

Epifascicular nucleus

icp:

Inferior cerebellar peduncle

IO:

Inferior olive

-ir:

Immunoreactive

I8:

Interstitial nucleus of the eighth nerve

LVe:

Lateral vestibular nucleus

mlf:

Medial longitudinal fasciculus

MVe:

Medial vestibular nucleus

nNos:

Nitric oxide synthase

NPNFP:

Nonphosphorylated neurofilament protein

PMD:

Nucleus paramedianus dorsalis

PMn:

Paramedian reticular nucleus

PrH:

Nucleus prepositus hypoglossi

PV:

Parvalbumin

RF:

Reticular formation

Ro:

Nucleus of Roller

SGe:

Suprageniculate nucleus

Sp5:

Spinal tract of the trigeminal

SpVe:

Inferior vestibular nucleus

Sub:

Subtrigeminal nucleus

SuVe:

Superior vestibular nucleus

6N:

Abducens nucleus

7n:

Seventh (facial) cranial nerve

8n:

Eighth cranial nerve

12N:

Nucleus of the hypoglossal nerve

References

  • Baizer JS (2009) Nonphosphorylated neurofilament protein is expressed by scattered neurons in the vestibular and precerebellar brainstem. Brain Res 1298:46–56

    Article  PubMed  CAS  Google Scholar 

  • Baizer JS, Baker JF (2005) Immunoreactivity for calcium-binding proteins defines subregions of the vestibular nuclear complex of the cat. Exp Brain Res 164:78–91

    Article  PubMed  CAS  Google Scholar 

  • Baizer JS, Baker JF (2006a) Immunoreactivity for calretinin and calbindin in the vestibular nuclear complex of the monkey. Exp Brain Res 172:103–113

    Article  PubMed  CAS  Google Scholar 

  • Baizer JS, Baker JF (2006b) Neurochemically defined cell columns in the nucleus prepositus hypoglossi of the cat and monkey. Brain Res 1094:127–137

    Article  PubMed  CAS  Google Scholar 

  • Baizer JS, Broussard DM (2010) Expression of calcium-binding proteins and nNOS in the human vestibular and precerebellar brainstem. J Comp Neurol 518:872–895

    Article  PubMed  CAS  Google Scholar 

  • Baizer JS, Baker JF, Haas K, Lima R (2007) Neurochemical organization of the nucleus paramedianus dorsalis in the human. Brain Res 1176:45–52

    Article  PubMed  CAS  Google Scholar 

  • Baizer JS, Corwin WL, Baker JF (2010a) Otolith stimulation induces c-Fos expression in vestibular and precerebellar nuclei in cats and squirrel monkeys. Brain Res 1351:64–73

    Article  PubMed  CAS  Google Scholar 

  • Baizer JS, Paolone N, Kramer V, Sherwood CC, Hof PR (2010b) Neurochemical organization of the chimpanzee vestibular brainstem. Soc Neurosci Abs 583.23/WW16

  • Baizer JS, Paolone NA, Witelson SF (2011a) Nonphosphorylated neurofilament protein is expressed by scattered neurons in the human vestibular brainstem. Brain Res 1382:45–56

    Article  PubMed  CAS  Google Scholar 

  • Baizer JS, Sherwood CC, Hof PR, Witelson SF, Sultan F (2011b) Neurochemical and structural organization of the principal nucleus of the inferior olive in the human. Anat Rec 294:1198–1216

    Article  CAS  Google Scholar 

  • Baizer JS, Weinstock N, Witelson SF, Sherwood CC, Hof PR (2012) The nucleus pararaphales in the human, chimpanzee, and macaque monkey. Brain Struct Funct. doi:10.1007/s00429-012-0403-8

  • Bakker DA, Richmond FJ, Abrahams VC, Courville J (1985) Patterns of primary afferent termination in the external cuneate nucleus from cervical axial muscles in the cat. J Comp Neurol 241:467–479

    Article  PubMed  CAS  Google Scholar 

  • Barmack NH (2003) Central vestibular system: vestibular nuclei and posterior cerebellum. Brain Res Bull 60:511–541

    Article  PubMed  Google Scholar 

  • Belknap DB, McCrea RA (1988) Anatomical connections of the prepositus and abducens nuclei in the squirrel monkey. J Comp Neurol 268:13–28

    Article  PubMed  CAS  Google Scholar 

  • Berman A (1968) The brain stem of the cat. University of Wisconsin Press, Madison

    Google Scholar 

  • Boyle R (2000) Morphology of lumbar-projecting lateral vestibulospinal neurons in the brainstem and cervical spinal cord in the squirrel monkey. Arch Ital Biol 138:107–122

    PubMed  CAS  Google Scholar 

  • Boyle R, Goldberg JM, Highstein SM (1992) Inputs from regularly and irregularly discharging vestibular nerve afferents to secondary neurons in squirrel monkey vestibular nuclei. III. Correlation with vestibulospinal and vestibuloocular output pathways. J Neurophysiol 68:471–484

    PubMed  CAS  Google Scholar 

  • Brodal A (1983) The perihypoglossal nuclei in the macaque monkey and the chimpanzee. J Comp Neurol 218:257–269

    Article  PubMed  CAS  Google Scholar 

  • Brodal A (1984) The vestibular nuclei in the macaque monkey. J Comp Neurol 227:252–266

    Article  PubMed  CAS  Google Scholar 

  • Brodal A, Pompeiano O (1957) The vestibular nuclei in cat. J Anat 91:438–454

    PubMed  CAS  Google Scholar 

  • Büttner-Ennever JA (1992) Patterns of connectivity in the vestibular nuclei. Ann N Y Acad Sci 656:363–378

    Article  PubMed  Google Scholar 

  • Carleton SC, Carpenter MB (1983) Afferent and efferent connections of the medial, inferior and lateral vestibular nuclei in the cat and monkey. Brain Res 278:29–51

    Article  PubMed  CAS  Google Scholar 

  • Carvalho S, Biro D, Cunha E, Hockings K, McGrew W, Richmond B, Matsuzawa T (2012) Chimpanzee carrying behaviour and the origins of human bipedality. Curr Biol 22:R180

    Article  PubMed  CAS  Google Scholar 

  • Changizi MA, Shimojo S (2005) Parcellation and area–area connectivity as a function of neocortex size. Brain Behav Evol 66:88–98

    Article  PubMed  Google Scholar 

  • Chen FC, Vallender EJ, Wang H, Tzeng CS, Li WH (2001) Genomic divergence between human and chimpanzee estimated from large-scale alignments of genomic sequences. J Hered 92:481–489

    Article  PubMed  CAS  Google Scholar 

  • Diogo R, Richmond BG, Wood B (2012) Evolution and homologies of primate and modern human hand and forearm muscles, with notes on thumb movements and tool use. J Hum Evol 63:64–78

    Article  PubMed  Google Scholar 

  • Emmers R, Akert K (1963) A stereotaxic atlas of the brain of the squirrel monkey (Saimiri sciureus). University of Wisconsin Press, Madison

    Google Scholar 

  • Gerrits N (1990) Vestibular nuclear complex. In: The human nervous system. Academic Press, Philadelphia, pp 863–888

  • Gerrits NM, Voogd J, Nas WS (1985) Cerebellar and olivary projections of the external and rostral internal cuneate nuclei in the cat. Exp Brain Res 57:239–255

    Article  PubMed  CAS  Google Scholar 

  • Grillner S, Hongo T, Lund S (1970) The vestibulospinal tract. Effects on alpha-motoneurones in the lumbosacral spinal cord in the cat. Exp Brain Res 10:94–120

    Article  PubMed  CAS  Google Scholar 

  • Gunz P, Ramsier M, Kuhrig M, Hublin JJ, Spoor F (2012) The mammalian bony labyrinth reconsidered, introducing a comprehensive geometric morphometric approach. J Anat 220:529–543

    Article  PubMed  Google Scholar 

  • Halasi G, Bacskai T, Matesz C (2005) Connections of the superior vestibular nucleus with the oculomotor and red nuclei in the rat: an electron microscopic study. Brain Res Bull 66:532–535

    Article  PubMed  Google Scholar 

  • Herculano-Houzel S (2010) Coordinated scaling of cortical and cerebellar numbers of neurons. Front Neuroanat 4:12

    PubMed  Google Scholar 

  • Herculano-Houzel S (2012) The remarkable, yet not extraordinary, human brain as a scaled-up primate brain and its associated cost. Proc Natl Acad Sci USA 109(Suppl 1):10661–10668

    Article  PubMed  CAS  Google Scholar 

  • Herculano-Houzel S, Kaas JH (2011) Gorilla and orangutan brains conform to the primate cellular scaling rules: implications for human evolution. Brain Behav Evol 77:33–44

    Article  PubMed  Google Scholar 

  • Herrero L, Pardoe J, Cerminara NL, Apps R (2012) Spatial localization and projection densities of brainstem mossy fibre afferents to the forelimb C1 zone of the rat cerebellum. Eur J Neurosci 35:539–549

    Article  PubMed  Google Scholar 

  • Highstein SM, Holstein GR (2006) The anatomy of the vestibular nuclei. Prog Brain Res 151:157–203

    Article  PubMed  CAS  Google Scholar 

  • Hof PR, Morrison JH (1995) Neurofilament protein defines regional patterns of cortical organization in the macaque monkey visual system: a quantitative immunohistochemical analysis. J Comp Neurol 352:161–186

    Article  PubMed  CAS  Google Scholar 

  • Hof PR, Ungerleider LG, Webster MJ, Gattass R, Adams MM, Sailstad CA, Morrison JH (1996) Neurofilament protein is differentially distributed in subpopulations of corticocortical projection neurons in the macaque monkey visual pathways. J Comp Neurol 376:112–127

    Article  PubMed  CAS  Google Scholar 

  • Hof PR, Ungerleider LG, Adams MM, Webster MJ, Gattass R, Blumberg DM, Morrison JH (1997) Callosally projecting neurons in the macaque monkey V1/V2 border are enriched in nonphosphorylated neurofilament protein. Vis Neurosci 14:981–987

    Article  PubMed  CAS  Google Scholar 

  • Jeffery N, Spoor F (2006) The primate subarcuate fossa and its relationship to the semicircular canals part I: prenatal growth. J Hum Evol 51:537–549

    Article  PubMed  Google Scholar 

  • Jeffery N, Ryan TM, Spoor F (2008) The primate subarcuate fossa and its relationship to the semicircular canals part II: adult interspecific variation. J Hum Evol 55:326–339

    Article  PubMed  Google Scholar 

  • Kaneko CR (1997) Eye movement deficits after ibotenic acid lesions of the nucleus prepositus hypoglossi in monkeys. I. Saccades and fixation. J Neurophysiol 78:1753–1768

    PubMed  CAS  Google Scholar 

  • Kaneko CR (1999) Eye movement deficits following ibotenic acid lesions of the nucleus prepositus hypoglossi in monkeys II. Pursuit, vestibular, and optokinetic responses. J Neurophysiol 81:668–681

    PubMed  CAS  Google Scholar 

  • Kitajima N, Sugita-Kitajima A, Bai R, Sasaki M, Sato H, Imagawa M, Kawamoto E, Suzuki M, Uchino Y (2006) Axonal pathways and projection levels of anterior semicircular canal nerve-activated vestibulospinal neurons in cats. Neurosci Lett 406:1–5

    Article  PubMed  CAS  Google Scholar 

  • Krubitzer L, Kaas J (2005) The evolution of the neocortex in mammals: how is phenotypic diversity generated? Curr Opin Neurobiol 15:444–453

    Article  PubMed  CAS  Google Scholar 

  • Kushiro K, Bai R, Kitajima N, Sugita-Kitajima A, Uchino Y (2008) Properties and axonal trajectories of posterior semicircular canal nerve-activated vestibulospinal neurons. Exp Brain Res 191:257–264

    Article  PubMed  Google Scholar 

  • LaBossiere E, Glickstein M (1976) Histological processing for the neural sciences. Charles C. Thomas, Springfield

    Google Scholar 

  • Langer T, Fuchs AF, Chubb MC, Scudder CA, Lisberger SG (1985a) Floccular efferents in the rhesus macaque as revealed by autoradiography and horseradish peroxidase. J Comp Neurol 235:26–37

    Article  PubMed  CAS  Google Scholar 

  • Langer T, Fuchs AF, Scudder CA, Chubb MC (1985b) Afferents to the flocculus of the cerebellum in the rhesus macaque as revealed by retrograde transport of horseradish peroxidase. J Comp Neurol 235:1–25

    Article  PubMed  CAS  Google Scholar 

  • Lovejoy CO (1988) Evolution of human walking. Sci Am 259:118–125

    Article  PubMed  CAS  Google Scholar 

  • MacLeod CE, Zilles K, Schleicher A, Rilling JK, Gibson KR (2003) Expansion of the neocerebellum in Hominoidea. J Hum Evol 44:401–429

    Article  PubMed  Google Scholar 

  • Mitsacos A, Reisine H, Highstein SM (1983) The superior vestibular nucleus: an intracellular HRP study in the cat. I. Vestibulo-ocular neurons. J Comp Neurol 215:78–91

    Article  PubMed  CAS  Google Scholar 

  • Olszewski J, Baxter D (1954) Cytoarchitecture of the human brain stem, 2nd edn. Karger, Basel

    Google Scholar 

  • Paxinos G, Huang XF (1995) Atlas of the human brainstem. Academic Press, San Diego

    Google Scholar 

  • Paxinos G, Watson C (1997) The rat brain, in stereotaxic coordinates, compact, 3rd edn. Academic Press, San Diego

    Google Scholar 

  • Paxinos G, Watson C (2007) The rat brain in stereotaxic coordinates, 6th edn. Academic Press/Elsevier, Amsterdam

    Google Scholar 

  • Paxinos G, Huang XF, Toga AW (2000) The rhesus monkey brain in stereotaxic coordinates. Academic Press, San Diego

    Google Scholar 

  • Pompeiano O, d’Ascanio P, Centini C, Pompeiano M, Balaban E (2002) Gene expression in rat vestibular and reticular structures during and after space flight. Neuroscience 114:135–155

    Article  PubMed  CAS  Google Scholar 

  • Preuss TM (2011) The human brain: rewired and running hot. Ann N Y Acad Sci 1225(Suppl 1):E182–E191

    Article  PubMed  Google Scholar 

  • Richmond BG, Jungers WL (2008) Orrorin tugenensis femoral morphology and the evolution of hominin bipedalism. Science 319:1662–1665

    Article  PubMed  CAS  Google Scholar 

  • Roste GK (1989) Observations on the projection from the perihypoglossal nuclei to the cerebellar cortex and nuclei in the cat. A retrograde WGA-HRP and fluorescent tracer study. Anat Embryol (Berl) 180:521–533

    Article  CAS  Google Scholar 

  • Sadjadpour K, Brodal A (1968) The vestibular nuclei in man. A morphological study in the light of experimental findings in the cat. J Hirnforsch 10:299–323

    PubMed  CAS  Google Scholar 

  • Schonewille M, Luo C, Ruigrok TJ, Voogd J, Schmolesky MT, Rutteman M, Hoebeek FE, De Jeu MT, De Zeeuw CI (2006) Zonal organization of the mouse flocculus: physiology, input, and output. J Comp Neurol 497:670–682

    Article  PubMed  Google Scholar 

  • Shrewsbury MM, Marzke MW, Linscheid RL, Reece SP (2003) Comparative morphology of the pollical distal phalanx. Am J Phys Anthropol 121:30–47

    Article  PubMed  CAS  Google Scholar 

  • Shu SY, Ju G, Fan LZ (1988) The glucose oxidase-DAB-nickel method in peroxidase histochemistry of the nervous system. Neurosci Lett 85:169–171

    Article  PubMed  CAS  Google Scholar 

  • Silcox MT, Bloch JI, Boyer DM, Godinot M, Ryan TM, Spoor F, Walker A (2009) Semicircular canal system in early primates. J Hum Evol 56:315–322

    Article  PubMed  Google Scholar 

  • Somana R, Walberg F (1980) A re-examination of the cerebellar projections from the gracile, main and external cuneate nuclei in the cat. Brain Res 186:33–42

    Article  PubMed  CAS  Google Scholar 

  • Spoor F, Garland T Jr, Krovitz G, Ryan TM, Silcox MT, Walker A (2007) The primate semicircular canal system and locomotion. Proc Natl Acad Sci USA 104:10808–10812

    Article  PubMed  CAS  Google Scholar 

  • Striedter GF (2005) Principles of brain evolution. Sinauer Associates, Sunderland

    Google Scholar 

  • Uchino Y, Sasaki M, Sato H, Bai R, Kawamoto E (2005) Otolith and canal integration on single vestibular neurons in cats. Exp Brain Res 164:271–285

    Article  PubMed  CAS  Google Scholar 

  • Van der Gucht E, Youakim M, Arckens L, Hof PR, Baizer JS (2006) Variations in the structure of the prelunate gyrus in Old World monkeys. Anat Rec 288:753–775

    Article  Google Scholar 

  • Ward CV, Plavcan JM, Manthi FK (2010) Anterior dental evolution in the Australopithecus anamensisafarensis lineage. Philos Trans R Soc Lond B Biol Sci 365:3333–3344

    Article  PubMed  Google Scholar 

  • Witelson SF, McCulloch PB (1991) Premortem and postmortem measurement to study structure with function: a human brain collection. Schizophr Bull 17:583–591

    Article  PubMed  CAS  Google Scholar 

  • Wood B, Richmond BG (2000) Human evolution: taxonomy and paleobiology. J Anat 197:19–60

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

Supported in part by the Department of Physiology and Biophysics, University at Buffalo and the James S. McDonnell Foundation, Grant 22002078 to CCS and PRH. We appreciate the assistance with data analysis of Jason Ng.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Joan S. Baizer.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Baizer, J.S., Paolone, N.A., Sherwood, C.C. et al. Neurochemical organization of the vestibular brainstem in the common chimpanzee (Pan troglodytes). Brain Struct Funct 218, 1463–1485 (2013). https://doi.org/10.1007/s00429-012-0470-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00429-012-0470-x

Keywords

Navigation