Both visual and idiothetic cues contribute to head direction cell stability during navigation along complex routes
Open accessAbstract
Successful navigation requires a constantly updated neural representation of directional heading, which is conveyed by head direction (HD) cells. The HD signal is predominantly controlled by visual landmarks, but when familiar landmarks are unavailable, self-motion cues are able to control the HD signal via path integration. Previous studies of the relationship between HD cell activity and path integration have been limited to two or more arenas located in the same room, a drawback for interpretation because the same visual cues may have been perceptible across arenas. To address this issue, we tested the relationship between HD cell activity and path integration by recording HD cells while rats navigated within a 14-unit T-maze and in a multiroom maze that consisted of unique arenas that were located in different rooms but connected by a passageway. In the 14-unit T-maze, the HD signal remained relatively stable between the start and goal boxes, with the preferred firing directions usually shifting <45° during maze traversal. In the multiroom maze in light, the preferred firing directions also remained relatively constant between rooms, but with greater variability than in the 14-unit maze. In darkness, HD cell preferred firing directions showed marginally more variability between rooms than in the lighted condition. Overall, the results indicate that self-motion cues are capable of maintaining the HD cell signal in the absence of familiar visual cues, although there are limits to its accuracy. In addition, visual information, even when unfamiliar, can increase the precision of directional perception.
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A possible solution is to use one's perceived orientation relative to local landmarks to anchor one's sense of direction, which can then be maintained during navigation through idiothetic cues.
“A possible solution is to use one’s perceived orientation relative to local (currently-visible) landmarks to anchor one’s sense of direction, which can then be maintained during navigation through idiothetic cues10–12.”
From Anchoring the neural compass: coding of local spatial reference frames in human medial parietal lobe (2014) · cites this paper as [11]
HD cells maintain stable preferred directions when traveling across distinct environments.
“the fact that HD cells maintain stable preferred directions when traveling across distinct environments11, 35, 36”
From Anchoring the neural compass: coding of local spatial reference frames in human medial parietal lobe (2014) · cites this paper as [11]
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Cites
Circular Statistics in Biology
Watson, G. S., & Batschelet, E. (1982) · Technometrics · doi:10.2307/1267831 · Cited by 4,573 · see citing works
Microstructure of a spatial map in the entorhinal cortex
Hafting, T., Fyhn, M., Molden, S., Moser, M.-B., & Moser, E. I. (2005) · Nature · doi:10.1038/nature03721 · Cited by 4,068 · see citing works
Taube, J., Muller, R., & Ranck, J. (1990) · The Journal of Neuroscience · doi:10.1523/jneurosci.10-02-00420.1990 · Cited by 1,809 · see citing works
Self-citationA purely geometric module in the rat's spatial representation
Cheng, K. (1986) · Cognition · doi:10.1016/0010-0277(86)90041-7 · Cited by 1,182 · see citing works
Zhang, K. (1996) · The Journal of Neuroscience · doi:10.1523/jneurosci.16-06-02112.1996 · Cited by 1,001 · see citing works
The Head Direction Signal: Origins and Sensory-Motor Integration
Taube, J. S. (2007) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.29.051605.112854 · Cited by 916 · see citing works
Self-citationTaube, J. S., Muller, R., & Ranck, J. B. (1990) · Journal of Neuroscience · doi:10.1523/jneurosci.10-02-00436.1990 · Cited by 887 · see citing works
Self-citationEtienne, A. S., & Jeffery, K. J. (2004) · Hippocampus · doi:10.1002/hipo.10173 · Cited by 726 · see citing works
Head direction cells recorded in the anterior thalamic nuclei of freely moving rats
Taube, J. S. (1995) · Journal of Neuroscience · doi:10.1523/jneurosci.15-01-00070.1995 · Cited by 688 · see citing works
Self-citationPlace cells, head direction cells, and the learning of landmark stability
Knierim, J., Kudrimoti, H., & McNaughton, B. (1995) · The Journal of Neuroscience · doi:10.1523/jneurosci.15-03-01648.1995 · Cited by 608 · see citing works
Introduction and removal of reward, and maze performance in rats.
Tolman, E. C., & Honzik, C. H. (1930) · Cited by 447 · see citing works
Path Integration in Mammals and its Interaction With Visual Landmarks
Etienne, A. S., Maurer, R., & Séguinot, V. (1996) · Journal of Experimental Biology · doi:10.1242/jeb.199.1.201 · Cited by 387 · see citing works
Distinct Representations and Theta Dynamics in Dorsal and Ventral Hippocampus
Royer, S., Sirota, A., Patel, J., & Buzsáki, G. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.4681-09.2010 · Cited by 341 · see citing works
Fragmentation of grid cell maps in a multicompartment environment
Derdikman, D., Whitlock, J. R., Tsao, A., Fyhn, M., Hafting, T., Moser, M.-B., & Moser, E. I. (2009) · Nature Neuroscience · doi:10.1038/nn.2396 · Cited by 330 · see citing works
Stackman, R. W., & Taube, J. S. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-21-09020.1998 · Cited by 304 · see citing works
Self-citationKnierim, J. J., Kudrimoti, H. S., & McNaughton, B. L. (1998) · Journal of Neurophysiology · doi:10.1152/jn.1998.80.1.425 · Cited by 297 · see citing works
van Groen, T., & Wyss, J. M. (1990) · Brain Research · doi:10.1016/0006-8993(90)90824-u · Cited by 254 · see citing works
Head direction cell activity monitored in a novel environment and during a cue conflict situation
Taube, J. S., & Burton, H. L. (1995) · Journal of Neurophysiology · doi:10.1152/jn.1995.74.5.1953 · Cited by 242 · cited 3× · see citing works
“This factor may explain the predominantly clockwise (CW) shifts observed in the preferred firing direction when rats made two overall CW 90° turns during their journey between familiar and novel arenas in previous studies (Stackman et al. 2003; Taube and Burton 1995).”
Self-citationThe anatomical and computational basis of the rat head-direction cell signal
Sharp, P. E., Blair, H. T., & Cho, J. (2001) · Trends in Neurosciences · doi:10.1016/s0166-2236(00)01797-5 · Cited by 236 · see citing works
Cue control and head direction cells.
Goodridge, J. P., Dudchenko, P. A., Worboys, K. A., Golob, E. J., & Taube, J. S. (1998) · Behavioral Neuroscience · doi:10.1037/0735-7044.112.4.749 · Cited by 229 · see citing works
Self-citationThe role of central and peripheral vision in perceiving the direction of self-motion
Warren, W. H., & Kurtz, K. J. (1992) · Perception & Psychophysics · doi:10.3758/bf03211640 · Cited by 228 · see citing works
Path Integration from Optic Flow and Body Senses in a Homing Task
Kearns, M. J., Warren, W. H., Duchon, A. P., & Tarr, M. J. (2002) · Perception · doi:10.1068/p3311 · Cited by 214 · see citing works
A driveable bundle of microwires for collecting single-unit data from freely-moving rats
Kubie, J. L. (1984) · Physiology & Behavior · doi:10.1016/0031-9384(84)90080-5 · Cited by 191 · see citing works
Direct projections from the anterior thalamic nuclei to the retrohippocampal region in the rat
Shibata, H. (1993) · The Journal of Comparative Neurology · doi:10.1002/cne.903370307 · Cited by 188 · see citing works
The effect of change of reward on the maze performance of rats
Elliott, M. H. (1928) · University of California Press eBooks · Cited by 158 · see citing works
Mechanisms of animal global navigation: comparative perspectives and enduring challenges
Bingman, V. P., & Cheng, K. (2005) · Ethology Ecology & Evolution · doi:10.1080/08927014.2005.9522584 · Cited by 152 · see citing works
Spatial memory in large scale movements: Efficiency and limitation of the egocentric coding process
Benhamou, S., Sauve, J.-P., & Bovet, P. (1990) · Journal of Theoretical Biology · doi:10.1016/s0022-5193(05)80531-4 · Cited by 141 · see citing works
Passive Transport Disrupts Directional Path Integration by Rat Head Direction Cells
Stackman, R. W., Golob, E. J., Bassett, J. P., & Taube, J. S. (2003) · Journal of Neurophysiology · doi:10.1152/jn.00346.2003 · Cited by 139 · see citing works
Self-citationPreferential use of the landmark navigational system by head direction cells in rats.
Goodridge, J. P., & Taube, J. S. (1995) · Behavioral Neuroscience · doi:10.1037//0735-7044.109.1.49 · Cited by 137 · see citing works
Self-citationVisual and vestibular influences on head-direction cells in the anterior thalamus of the rat.
Blair, H. T., & Sharp, P. E. (1996) · Behavioral Neuroscience · doi:10.1037/0735-7044.110.4.643 · Cited by 132 · see citing works
Visual and vestibular influences on head-direction cells in the anterior thalamus of the rat.
Blair, H. T., & Sharp, P. E. (1996) · Behavioral Neuroscience · doi:10.1037//0735-7044.110.4.643 · Cited by 131 · see citing works
Bassett, J. P., Tullman, M. L., & Taube, J. S. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.0268-07.2007 · Cited by 125 · see citing works
Self-citationPreferential use of the landmark navigational system by head direction cells in rats.
Goodridge, J. P., & Taube, J. S. (1995) · Behavioral Neuroscience · doi:10.1037/0735-7044.109.1.49 · Cited by 115 · see citing works
Self-citationDead reckoning in a small mammal: the evaluation of distance
S�guinot, V., Maurer, R., & Etienne, A. S. (1993) · Journal of Comparative Physiology A · doi:10.1007/bf00209622 · Cited by 111 · see citing works
Resetting the path integrator: a basic condition for route-based navigation
Etienne, A. S., Maurer, R., Boulens, V., Lévy, A., & Rowe, T. (2004) · Journal of Experimental Biology · doi:10.1242/jeb.00906 · Cited by 105 · see citing works
Rapid Spatial Reorientation and Head Direction Cells
Zugaro, M. B., Arleo, A., Berthoz, A., & Wiener, S. I. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-08-03478.2003 · Cited by 102 · see citing works
Homing in Virtual Environments: Effects of Field of View and Path Layout
Péruch, P., May, M., & Wartenberg, F. (1997) · Perception · doi:10.1068/p260301 · Cited by 88 · see citing works
Piloting and dead reckoning dissociated by fimbria-fornix lesions in a rat food carrying task
Whishaw, I. Q., & Tomie, J.-A. (1997) · Behavioural Brain Research · doi:10.1016/s0166-4328(97)00068-5 · Cited by 83 · see citing works
Singer, A. C., Karlsson, M. P., Nathe, A. R., Carr, M. F., & Frank, L. M. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.0926-10.2010 · Cited by 80 · see citing works
Frohardt, R. J., Bassett, J. P., & Taube, J. S. (2006) · Behavioral Neuroscience · doi:10.1037/0735-7044.120.1.135 · Cited by 76 · see citing works
Self-citationThe Ecological Approach to Navigation: A Gibsonian Perspective
Heft, H. (2007) · Springer eBooks · doi:10.1007/978-0-585-33485-1_6 · Cited by 69 · see citing works
Istomin, K. V., & Dwyer, M. J. (2009) · Current Anthropology · doi:10.1086/595624 · Cited by 61 · see citing works
Clark, B. J., Harris, M., & Taube, J. S. (2010) · Hippocampus · doi:10.1002/hipo.20880 · Cited by 48 · see citing works
Self-citationInfluence of conflicting visual, inertial and substratal cues on head direction cell activity
Zugaro, M., Tabuchi, E., & Wiener, S. I. (2000) · Experimental Brain Research · doi:10.1007/s002210000365 · Cited by 48 · see citing works
A brief view of known landmarks reorientates path integration in hamsters
Etienne, A. S., Boulens, V., Maurer, R., Rowe, T., & Siegrist, C. (2000) · Die Naturwissenschaften · doi:10.1007/s001140050766 · Cited by 45 · see citing works
Dudchenko, P. A., & Zinyuk, L. E. (2005) · Behavioral Neuroscience · doi:10.1037/0735-7044.119.6.1511 · Cited by 41 · see citing works
Human Path Integration by Optic Flow
Ellmore, T. M., & McNaughton, B. L. (2004) · Spatial Cognition and Computation · doi:10.1207/s15427633scc0403_3 · Cited by 40 · see citing works
Deficits in landmark navigation and path integration after lesions of the interpeduncular nucleus.
Clark, B. J., & Taube, J. S. (2009) · Behavioral Neuroscience · doi:10.1037/a0015477 · Cited by 36 · see citing works
Self-citationRole of optical flow field asymmetry in the perception of heading during linear motion
Telford, L., & Howard, I. P. (1996) · Perception & Psychophysics · doi:10.3758/bf03211881 · Cited by 17 · see citing works
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Anchoring the neural compass: coding of local spatial reference frames in human medial parietal lobe
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Hulse, B. K., & Jayaraman, V. (2020) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-072116-031516 · Cited by 130 · see citing works
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- Authors
- Yoder, R. M., Clark, B. J., Brown, J. E., Lamia, M. V., Valerio, S., Shinder, M. E., & Taube, J. S.
- Affiliations
- Dartmouth College (US)
- Department of Psychological and Brain Sciences, Center for Cognitive Neuroscience, Dartmouth College, Hanover, New Hampshire
- Corresponding author
- Taube, Jeffrey S.
- Venue
- Journal of Neurophysiology
- Publisher
- American Physiological Society
- Published
- 2011-06
- Volume
- 105
- Issue
- 6
- Pages
- 2989-3001
- ISSN
- 0022-3077 (ISSN-L)
- 1522-1598
- PMC
- PMC3118751
- OpenAlex
- W1970755914
- Cited by
- 105
- References
- 49
- Citations by year
- 2026: 4 · 2025: 3 · 2024: 28 · 2023: 7 · 2022: 2 · 2021: 4 · 2020: 7 · 2019: 4 · 2018: 6 · 2017: 8 · 2016: 7 · 2015: 4 · 2014: 12 · 2013: 2 · 2012: 6
- FWCI
- 3.41
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Journal of Neurophysiology (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Opus: Research & Creativity (Indiana University – Purdue University Fort Wayne) (submittedVersion)
- Funders
- U.S. Public Health Service
- National Institute on Deafness and Other Communication Disorders (F32DC008481, DC009318, DC008773, R01DC009318, F32DC008773, DC008481)
- National Institute of Neurological Disorders and Stroke (NS 053907)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Physical Sciences › Engineering › Automotive Engineering › Spatial Cognition and Navigation
- Life Sciences › Neuroscience › Neurology › Vestibular and auditory disorders
- Keywords
- head direction cells, path integration, self-motion cues, idiothetic cues, visual landmarks, spatial navigation, T-maze, darkness, rats, heading stability
- MeSH terms
- Action Potentials, Animals, Brain, Cues, Dark Adaptation, Female, Neurons, Photic Stimulation, Space Perception, Spectrum Analysis, Maze Learning, Head Movements, Rats, Long-Evans, Rats
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