link.springer.com

Head-direction cells in the rat posterior cortex - Experimental Brain Research

  • ️McNaughton, Brace L.
  • ️Thu Sep 01 1994

Abstract

This study investigated the effects of visual and ideothetica cues on the spatial tuning of head-direction (HD) cells recorded in the rat posterior cortices. Extracellular, single unit responses were recorded from animals performing each of two different tasks, a spatial working memory task on a radial-arm maze and a passive rotation task on a modified “lazy Susan” platform. The influence of visual cues was assessed by manipulating the position of one white and three black cue-cards placed around the maze. We found three major categories of HD cells based on their response to cue manipulations in the maze tasks. Type A cells (10/41) rotated their preferred directions along with the rotation of the cues. The majority (type B, 25/41) of the HD cells were unaffected by the rotation of visual cues, maintaining their established preferred direction. Type C cells (6/41) showed complex responses to cue rotation, with the preferred direction reflecting either a combination of both type A and type B responses or an unpredictable response. The results indicate that the internal representation of directionality can be calibrated by visual cues and that some mnemonic processes may have been involved in the registration of the previous cue locations. Eleven cells were tested in both the maze task and the passive rotation task. Most (9/11) showed a significant directionality in the former task, but showed either no or weak directionality in the latter task, suggesting that movement-related ideothetic cues may be used in supporting the directional firing of these cells. Only two cells showed significant directionality in both tasks. Their established preferred directions did not rotate along with the cues in the maze task, but did rotate with the cues in the passive rotation task. We conclude that the dynamic aspect of the directional tuning in these cortical HD cells may represent on-line calibration of an angular coordinate representation.

Access this article

Log in via an institution

Subscribe and save

  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Andersen RA, Mountcastle VB (1983) The influence of the angle of gaze upon the excitability of the light-sensitive neurons of the posterior parietal cortex. J Neurosci 3:532–548

    Google Scholar 

  • Andersen RA, Essick GK, Siegel RM (1985) Encoding of spatial location by posterior parietal neurons. Science 230:456–458

    Google Scholar 

  • Birch D, Jacobs GH (1969) Spatial contrast sensitivity in albino and pigmented rats. Vision Res 19:933–937

    Google Scholar 

  • Chen LL (1991) Head-directional information processing in the rat posterior cortical areas. PhD dissertation. University of Colorado, Boulder, CO

    Google Scholar 

  • Chen LL, McNaughton BL (1988) Spatially selective discharge of vision and movement modulated posterior parietal neurons in the rat. Soc Neurosci Abstr 14:818

    PubMed  Google Scholar 

  • Chen LL, McNaughton BL, Barnes CA, Ortiz ER (1990) Head-directional and behavioral correlates of posterior cingulate and medial prestriate cortex neurons in freely-moving rats. Soc Neurosci Abstr 16:441

    Google Scholar 

  • Chen LL, Lin L-H, McNaughton BL, Barnes CA, Gibbons DF (1991) Progressive decrease of behavioral modulation of head-direction cells from medial prestriate cortex to retrosplenial cortex. Soc Neurosci Abstr 17:1395

    Google Scholar 

  • Chen LL, Lin L-H, Green EJ, Barnes CA, McNaughton BL (1994) Head-direction cells in the rat posterior cortex. I. Anatomical distribution and behavioral modulation. Exp Brain Res 101:8–23

    CAS  PubMed  Google Scholar 

  • Etienne AS (1992) Navigation of a small mammal by dead reckoning and local cues. Curr Dir Psychol Sci 1:48–52

    Google Scholar 

  • Foster TC, Castro CA, McNaughton BL (1989) Spatial selectivity of hippocampal neurons: dependence on preparedness for movement. Science 24:1580–1582

    Google Scholar 

  • Gallistel CR (1990) The organization of learning. MIT press, Cambridge, MA

    Google Scholar 

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

    Google Scholar 

  • Groen T van, Wyss JM (1990b) Connections of the retrosplenial granular A cortex in the rat. J Comp Neurol 300:593–606

    Google Scholar 

  • Hyvarinen J (1982) The parietal cortex of monkey and man. Springer, Berlin Heidelberg New York

    Google Scholar 

  • Itaya SK, Van Hoesen GW, Jenq CB (1981) Direct retinal input to the limbic system of the rat. Brain Res 226:33–42

    Google Scholar 

  • McNaughton BL, O'Keefe J, Barnes CA (1983) The stereotrode: a new technique for simultaneous isolation of several single units in the central nervous system from multiple unit records. J Neurosci Methods 8:391–397

    Google Scholar 

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

    Google Scholar 

  • Miller MW, Vogt BA (1984) Direct connections of rat visual cortex with sensory, motor, and association cortices. J Comp Neurol 226:184–202

    Google Scholar 

  • Mittelstaedt ML, Glasauer S (1991) Ideothetic navigation in gerbils and humans. Zool J Physiol 95:427–435

    Google Scholar 

  • Mittelstaedt ML, Mittelstaedt H (1980) Homing by path integration in a mammal. Naturwissenschaften 67:566

    Google Scholar 

  • Newsome WT, Wurtz RH, Dursteler MR, Mikami A (1988) Relation of cortical areas MT and MST to pursuit eye movements. II. Differentiation of retinal from extraretinal inputs. J Neurophysiol 60:604–620

    Google Scholar 

  • Ohzawa I, DeAngelis GC, Freeman RD (1990) Stereoscopic depth discrimination in the visual cortex: neurons ideally suited as disparity detectors. Nature 249:1037–1041

    Google Scholar 

  • Poggio GF, Gonzalez F, Krause F (1988) Stereoscopic mechanisms in monkey visual cortex: binocular correlation an disparity selectivity. J Neurosci 8:4531–4550

    Google Scholar 

  • Ranck JB (1984) Head-direction cells in the deep cell layer of dorsal presubiculum in freely moving rats. Soc Neurosci Abstr 10:599

    Google Scholar 

  • Robinson DL, Wurtz RH (1976) Use of an extraretinal signal by monkey superior colliculus neurons to distinguish real from self-induced stimulus movement. J Neurophysiol 39:852–870

    Google Scholar 

  • Robinson EW, Wever EG (1930) Visual distance perception in the rat. University of California. Publications in Psychology 4:233–239

    Google Scholar 

  • Sakata H, Shibutani H, Kawano K, Harrington TL (1985) Neural mechanisms of space vision in the parietal association cortex of the monkey. Vision Res 25:453–463

    Google Scholar 

  • Sharp PE, Kubie JL, Muller RU (1990) Firing properties of hippocampal neurons in a visually symmetrical environment: contribution of multiple sensory cues and mnemonic processes. J Neurosci 10:3093–3105

    Google Scholar 

  • Sparks DL, Mays LE (1990) Signal transformations required for the generation of saccadic eye movements. Annu Rev Neurosci 13:309–336

    Google Scholar 

  • Sripanidkulchai K, Wyss JM (1986) Thalamic projections of retrosplenial cortex in the rat. J Comp Neurol 254:143–165

    Google Scholar 

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

    Google Scholar 

  • Thompson SM, Robertson RT (1987) Organization of subcortical pathways for sensory projections to the limbic cortex I. Subcortical projections to the medial limbic cortex in the rat. J Comp Neurol 265:175–188

    Google Scholar 

  • Toldi J, Foher O, Wolff JR (1986) Sensory interactive zones in the rat cerebral cortex. Neuroscience 2:461–465

    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

    Google Scholar 

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

    Google Scholar 

  • Wiesenfeld Z, Branchek T (1976) Refractive state and visual acuity in the hooded rat. Vision Res 16:823–827

    Google Scholar 

  • Wyss JM, Groen T van (1992) Connections between the retrosplenial cortex and the hippocampal formation in the rat. Hippocampus 2:1–11

    Google Scholar 

  • Zipser D, Andersen RA (1988) A back-propagation programmed network that simulates response properties of a subset of posterior parietal neurons. Nature 331:679–684

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Author notes

  1. Longtang L. Chen

    Present address: Laboratory for Neural Information Processing, RIKEN, 2-1 Hirosawa, 351-01, Saitama, Japan

  2. Lie-Huey Lin

    Present address: Laboratory of Neurogenetics, NIAAA, 12501 Washington Ave, 20852, Rockville, MD, USA

Authors and Affiliations

  1. Behavioral Neuroscience Program, University of Colorado, 80309, Boulder, CO, USA

    Longtang L. Chen

  2. ARL Division of Neural System, Memory and Aging, University of Arizona, 85724, Tucson, AZ, USA

    Lie-Huey Lin, Carol A. Barnes & Brace L. McNaughton

Authors

  1. Longtang L. Chen

    You can also search for this author in PubMed Google Scholar

  2. Lie-Huey Lin

    You can also search for this author in PubMed Google Scholar

  3. Carol A. Barnes

    You can also search for this author in PubMed Google Scholar

  4. Brace L. McNaughton

    You can also search for this author in PubMed Google Scholar

About this article

Cite this article

Chen, L.L., Lin, LH., Barnes, C.A. et al. Head-direction cells in the rat posterior cortex. Exp Brain Res 101, 24–34 (1994). https://doi.org/10.1007/BF00243213

Download citation

  • Received: 04 January 1993

  • Accepted: 01 February 1994

  • Issue Date: September 1994

  • DOI: https://doi.org/10.1007/BF00243213

Key words