Skip to main content

Sensory Determinants of Head Direction Cell Activity

  • Chapter
The Neural Basis of Navigation

Abstract

Other portions of this volume provide a description of the fundamental properties of Head Direction (HD) cells and the brain structures that are important in processing this directional coding (see the Preface and Chapter 9). This chapter focuses on the types of sensory information that affect HD cell activity. We first consider how cues external to the body can affect HD cell discharge and then discuss the efficacy of cues derived from the body’s movements (i.e., those involved in path integration; see Chapter 9). We then discuss experiments that have examined how HD cells respond when these two types of information come in conflict with one another. Because many animals function in a three-dimensional environment, we’ll also describe studies that have examined HD cell activity when the animal is in different earth-centered planes. Finally, we conclude by discussing experiments that have explored the development of cue control and spatial orientation as it relates to HD cells.

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

Access this chapter

eBook
USD 16.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 109.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 109.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Aguirre GK, Zarahn E, D’Esposito M (1998) An area within human ventral cortex sensitive to “building” stimuli: evidence and implications. Neuron 21: 373–383.

    Article  PubMed  Google Scholar 

  • Alyan SH, McNaughton BL (1999) Hippocampectomized rats are capable of homing by path integration. Beh Neurosci 113: 19–31.

    Article  Google Scholar 

  • Alyan SH, Jander R (1994) Short-range homing in the house mouse, Mus musculus: stages in the learning of directions. Animal Behav 48: 285–298.

    Article  Google Scholar 

  • Barlow JS (1964) Inertial navigation as a basis for animal navigation. J Theoretical Biol 6: 76–117.

    Article  Google Scholar 

  • Bassett JP, Taube JS (1999) Retrosplenial cortex lesions disrupt stability of head direction cell activity. Soc Neurosci Abstr 25: 1383.

    Google Scholar 

  • Bassett JP, Taube JS (2001) Neural correlates for angular head velocity in the rat dorsal tegmental nucleus. J Neurosci 21:5740–5751.

    PubMed  Google Scholar 

  • Biegler R, Morris RGM (1993) Landmark stability is a prerequisite for spatial but not discrimination learning. Nature 361: 631–633.

    Article  PubMed  Google Scholar 

  • Blair HT, Sharp PE (1996) Visual and vestibular influences on head-direction cells in the anterior thalamus of the rat. Behav Neurosci 110: 643–660.

    Article  PubMed  Google Scholar 

  • Calton JL, Tullman ML, Taube JS (2000) Head direction cell activity in the anterodorsal thalamus during upside-down locomotion. Soc Neurosci Abstr 26: 983.

    Google Scholar 

  • Calton JL, Taube JS (2001) Head direction cell activity following bilateral lesions of posterior parietal cortex. Soc Neurosci Abstr, in press.

    Google Scholar 

  • Chen LL, Lin LH, Barnes CA, McNaughton BL (1994) Head direction cells in the rat posterior cortex. II. Contributions of visual and ideothetic information to the directional firing. Exp Brain Res 101: 24–34.

    Article  PubMed  Google Scholar 

  • Cheng K (1986) A purely geometric module in the rat’s spatial representation. Cognition 23: 149–178.

    Article  PubMed  Google Scholar 

  • Dudchenko PA, Goodridge JP, Seiterle DA, Taube JS (1997a) Effects of repeated disorientation on the acquisition of two spatial reference memory tasks in rats: dissociation between the radial arm maze and the Morris water maze. J Exp Psych: Animal Behav Processes 23: 194–210.

    Article  Google Scholar 

  • Dudchenko PA, Goodridge JP, Taube JS (1997b) The effects of disorientation on visual landmark control of head direction cell orientation. Exp Brain Res 115: 375–380.

    Article  Google Scholar 

  • Dudchenko PA, Taube JS (1997) Correlation between head direction cell activity and spatial behavior on a radial arm maze. Behav Neurosci 111:3–19.

    Article  PubMed  Google Scholar 

  • Epstein R, Kanwisher N (1998) A cortical representation of the local visual environment. Nature 392: 568–601.

    Article  Google Scholar 

  • Etienne AS, Lambert SJ, Reverdin B, Teroni E (1993) Learning to recalibrate the role of dead reckoning and visual cues in spatial navigation. Animal Learn Beh 21: 266–280.

    Article  Google Scholar 

  • Etienne AS, Maurer R, Saucy F (1988) Limitations in the assessment of path dependent information. Behaviour 106:81–111.

    Article  Google Scholar 

  • Etienne AS, Maurer R, Seguinot V (1996) Path integration in mammals and its interaction with visual landmarks. J Exp Biol 199: 201–209.

    PubMed  Google Scholar 

  • Etienne AS, Teroni V, Hurni C, Protenier V (1990) The effect of a single light cue on homing behaviour of the golden hamster. Animal Beh 39: 17–41.

    Article  Google Scholar 

  • Gallistel CR (1990) The Organization of Learning. MIT Press: Cambridge, MA

    Google Scholar 

  • Golob EJ, Taube JS (1997) Head direction cells and episodic spatial information in rats without a hippocampus. Proc Natl Acad Sci (USA) 94: 7645–7650.

    Article  Google Scholar 

  • Golob EJ, Wolk DA, Taube JS (1998) Recordings of postsubicular head direction cells following lesions of the lateral dorsal thalamic nucleus. Brain Res 780: 9–19.

    Article  PubMed  Google Scholar 

  • Golob EJ, Taube JS (1999) Head direction cells in rats with hippocampal or overlying neocortical lesions: Evidence for impaired angular path integration. J Neurosci 19: 7198–7211.

    PubMed  Google Scholar 

  • Golob EJ, Stackman RW, Wong AC, Taube JS (2001) On the behavioral significance of head direction cells: Neural and behavioral dynamics during spatial memory tasks. Beh Neurosci 115:285–304.

    Article  Google Scholar 

  • Goodridge JP, Dudchenko PA, Worboys KA, Golob EJ, Taube JS (1998) Cue control and head direction cells. Beh Neurosci 112: 749–761.

    Article  Google Scholar 

  • Goodridge JP, Taube JS (1995) Preferential use of the landmark navigational system by head direction cells. Behav Neurosci 109: 49–61.

    Article  PubMed  Google Scholar 

  • Goodridge JP, Taube JS (1997) Interaction between postsubiculum and anterior thalamus in the generation of head direction cell activity. J Neurosci 17: 9315–9330.

    PubMed  Google Scholar 

  • Knierim JJ, Kudrimoti HS, McNaughton BL (1995) Place cells, head direction cells, and the learning of landmark stability. J Neurosci 15: 1648–1659.

    PubMed  Google Scholar 

  • Knierim JJ, Kudrimoti HS, McNaughton BL (1998) Interactions between idiothetic and external cues in the control of place cells and head direction cells. J Neurophysiol 80: 425–446.

    PubMed  Google Scholar 

  • Kubie JL, Ranck JB Jr (1983) Sensory-behavioral correlates in individual hippocampus neurons in three situations: space and context. In: Neurobiology of the Hippocampus, pp 433–447. Ed. W Seifert. Academic Press: New York, NY.

    Google Scholar 

  • Margules J, Gallistel CR (1988) Heading in the rat: determination by environmental shape. Animal Learn Behav 16: 404–410.

    Article  Google Scholar 

  • Martin GM, Harley CW, Smith AR, Hoyles ES, Hynes CA (1997) Opaque transportation with rotation blocks reliable goal location on a plus maze but does not prevent goal location in the Morris maze. J Exp Psych: Animal Behav Processes 23: 183–193.

    Article  Google Scholar 

  • McNaughton BL, Barnes CA, Gerrard JL, Gothard K, Jung MW, Knierim JJ, Kudrimoti H, Qin Y, Skaggs WE, Suster M, Weaver KL (1996) Deciphering the hippocampal polyglot: the hippocampus as a path integration system. J Exp Biol 199: 173–185.

    PubMed  Google Scholar 

  • McNaughton BL, Chen LL, Markus EJ (1991) “Dead reckoning,” landmark learning, and the sense of direction: a neurophysiological and computational hypothesis. J Cog Neurosci 3:190–202.

    Article  Google Scholar 

  • Miller VM, Best PJ (1980) Spatial correlates of hippocampal unit activity are altered by lesions of the fornix and entorhinal cortex. Brain Res 194: 311–323.

    Article  PubMed  Google Scholar 

  • Mizumori SJY, Cooper BG, Leutgeb S, Pratt W (2001) A neural systems analysis of adaptive navigation. Mol Neurobiol 21: 57–82.

    Article  Google Scholar 

  • Mizumori SJY, Williams JD (1993) Directionally selective mnemonic properties of neurons in the lateral dorsal nucleus of the thalamus of rats. J Neurosci 13: 4015–4028.

    PubMed  Google Scholar 

  • Oman CM (1990) Motion sickness: a synthesis and evaluation of the sensory conflict theory. Canad J Physiol Pharmacol 6: 294–303.

    Article  Google Scholar 

  • Poucet B (1993) Spatial cognitive maps in animals: new hypotheses on their structure and neural mechanisms. Psych Rev 100: 163–182.

    Article  Google Scholar 

  • Reason JT (1978) Motion sickness adaptation: a neural mismatch model. J Royal Soc Med 71: 819–829.

    Google Scholar 

  • Redish AD, Touretzky DS (1997) Cognitive maps beyond the hippocampus. Hippocampus 7: 15–35.

    Article  PubMed  Google Scholar 

  • Sharp PE, Cho J, Tinkelman A (2001) Angular velocity and head direction signals recorded from the dorsal tegmental nucleus of Gudden in the rat: Implications for path integration in the head direction cell circuit. Beh Neurosci 115: 571–588.

    Article  Google Scholar 

  • Stackman RW, Taube JS (1997) Firing properties of head direction cells in rat anterior thalamic neurons: dependence upon vestibular input. J Neurosci 17: 4349–4358.

    PubMed  Google Scholar 

  • Stackman RW, Taube JS (1998) Firing properties of rat lateral mammillary nuclei single units: head direction, head pitch, and angular head velocity, J Neurosci 18: 9020–9037.

    PubMed  Google Scholar 

  • Stackman RW, Tullman ML, Taube JS (2000) Maintenance of rat head direction cell firing during locomotion in the vertical plane. J Neurophysiol 83: 393–405.

    PubMed  Google Scholar 

  • Stackman RW, Clark AS, Taube JS (2001) Hippocampal spatial representations require vestibular input. Hippocampus, in press.

    Google Scholar 

  • Taube JS (1995) Head direction cells recorded in the anterior thalamic nuclei of freely moving rats. J Neurosci 15: 70–86.

    PubMed  Google Scholar 

  • Taube JS (1998) Head direction cells and the neurophysiological basis for a sense of direction. ProgNeurobiol 55:225–256.

    Google Scholar 

  • Taube JS, Burton HL (1995) Head direction cell activity monitored in a novel environment and during a cue conflict situation. J Neurophysiol 74: 1953–1971.

    PubMed  Google Scholar 

  • Taube JS, Goodridge JP, Golob EJ, Dudchenko PA, Stackman RW (1996) Processing the head direction cell signal: a review and commentary. Brain Res Bull 40: 477–486.

    Article  PubMed  Google Scholar 

  • Taube JS, Muller RU, Ranck JB Jr (1990a) Head-direction cells recorded from the postsubiculum in freely moving rats. I. Description and quantitative analysis. J Neurosci 10: 420–435.

    Google Scholar 

  • Taube JS, Muller RU, Ranck JB Jr (1990b) Head-direction cells recorded from the postsubiculum in freely moving rats. II. Effects of environmental manipulations. J Neurosci 10: 436–447.

    PubMed  Google Scholar 

  • Taube JS, Stackman RW, Dudchenko PA (1996) Head-direction cell activity monitored following passive transport into a novel environment. Soc Neurosci Abstr 22: 1873.

    Google Scholar 

  • Van Groen T, Wyss JM (1990) The postsubicular cortex in the rat: characterization of the fourth region of the subicular cortex and its connections. Brain Research, 529: 165–177.

    Article  PubMed  Google Scholar 

  • Vogt BA, Miller MW (1983) Cortical connections between rat cingulate cortex and visual, motor, and postsubicular cortices. J. Comp. Neurol., 216: 192–210.

    Article  PubMed  Google Scholar 

  • Whishaw IQ, McKenna JE, Maaswinkel H (1997) Hippocampal lesions and path integration. Current Opin Neurobiol 7: 228–234.

    Article  Google Scholar 

  • Wiener SI (1993) Spatial and behavioral correlates of striatal neurons in rats performing a self-initiated navigation task. J Neurosci 13: 3802–3817.

    PubMed  Google Scholar 

  • Zugaro MB, Tabuchi E, Wiener SI (2000) Influence of conflicting visual, inertial and substratal cues on head direction cell activity. Exp Brain Res 133: 198–208.

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jeffrey S. Taube .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2002 Springer Science+Business Media New York

About this chapter

Cite this chapter

Taube, J.S. (2002). Sensory Determinants of Head Direction Cell Activity. In: Sharp, P.E. (eds) The Neural Basis of Navigation. Springer, Boston, MA. https://doi.org/10.1007/978-1-4615-0887-8_8

Download citation

  • DOI: https://doi.org/10.1007/978-1-4615-0887-8_8

  • Publisher Name: Springer, Boston, MA

  • Print ISBN: 978-1-4613-5288-4

  • Online ISBN: 978-1-4615-0887-8

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics