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Cited by 1,809Memory and Neural MechanismsSpatial Cognition and NavigationVestibular and auditory disorders

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Head-direction cells recorded from the postsubiculum in freely moving rats. I. Description and quantitative analysis

Open access
Taube, JS, Muller, RU, Ranck, JB·1990·The Journal of Neuroscience
DOI 10.1523/jneurosci.10-02-00420.1990PMC PMC6570151
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Abstract

This paper is a study of the behavioral and spatial firing correlates of neurons in the rat postsubiculum. Recordings were made from postsubicular neurons as rats moved freely throughout a cylindrical chamber, where the major cue for orientation was a white card taped to the inside wall. An automatic video/computer system monitored cell discharge while simultaneously tracking the position of 2 colored light emitting diodes (LEDs) secured to the animal's head. The animal's location was calculated from the position of one of the LEDs and head direction in the horizontal plane calculated from the relative positions of the 2 LEDs. Approximately 26% of the cells were classified as head-direction cells because they discharged as a function of the animal's head direction in the horizontal plane, independent of the animal's behavior, location, or trunk position. For each head-direction cell, vectors drawn in the direction of maximal firing were parallel throughout the recording chamber and did not converge toward a single point. Plots of firing rate versus head direction showed that each firing-rate/head-direction function was adequately described by a triangular function. Each cell's maximum firing rate occurred at only one (the preferred) head direction; firing rates at head directions on either side of the preferred direction decreased linearly with angular deviation from the preferred direction. Results from 24 head-direction cells in 7 animals showed an equal distribution of preferred firing directions over a 360 degrees angle. The peak firing rate of head-direction cells varied from 5 to 115 spikes/sec (mean: 35). The range of head-direction angles over which discharge was elevated (directional firing range) was usually about 90 degrees, with little, if any, discharge at head directions outside this range. Quantitative analysis showed the location of the animal within the cylinder had minimal effect on directional cell firing. For each head-direction cell, the preferred direction, peak firing rate, and directional firing range remained stable for days. These results identify a new cell type that signals the animal's head direction in its environment.

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Crossref · 10.1523/jneurosci.10-02-00420.1990

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Figures

Image 1
CC-BY-NC-SA · From the PDF
Image 2
CC-BY-NC-SA · From the PDF
Image 3
CC-BY-NC-SA · From the PDF
Figure 3 Firing rate as a function of head direction for 3 representative cells from 3 different animals. Each plot is based on 8 min of recording, and head direction was analyzed with a 6° bin width. Note that the preferred direction and peak firing rate are different for each cell. A, Low-peak firing rate cell. B, Medium-peak firing rate cell. C, High-peak firing rate cell.
Figure 3 Firing rate as a function of head direction for 3 representative cells from 3 different animals. Each plot is based on 8 min of recording, and head direction was analyzed with a 6° bin width. Note that the preferred direction and peak firing rate are different for each cell. A, Low-peak firing rate cell. B, Medium-peak firing rate cell. C, High-peak firing rate cell.CC-BY-NC-SA · From the PDF
Figure 4 Summary of the triangular model of head-direction cell firing. The solid curve shows firing rate as a function of head direction for a typical head-direction cell. The 2 dashed lines, along with the base, form the triangle that was considered to best fit the raw data. The angle below the apex of the triangle is taken to be the preferred direction (118.5°). The peak firing rate is taken as the height of the triangle (80.2 spi s s s s sor the left leg. of the triangle (63.5º) to the X intercept of the right leg of the triangle (164.6°) and is 101.1°. The left leg of the triangle was obtained from a least-squares fit of the 9 data points between and including points A and B. The right leg of the triangle was obtained from a least-squares fit of the 7 data points between and including points C and D. The magnitude of the background firing rate (6.26 AP/sec) is indicated by the horizontal dotted line. The background firing rate was taken as the mean firing rate for all data points more than 18º counterclockwise from the X intercept of the left leg of the triangle and more than 18° clockwise from the X intercept of the right leg of the triangle (in this case, 39 points). The asymmetry of the triangle was defined as the absolute value of the left leg slope divided by the right leg slope.
Figure 4 Summary of the triangular model of head-direction cell firing. The solid curve shows firing rate as a function of head direction for a typical head-direction cell. The 2 dashed lines, along with the base, form the triangle that was considered to best fit the raw data. The angle below the apex of the triangle is taken to be the preferred direction (118.5°). The peak firing rate is taken as the height of the triangle (80.2 spi s s s s sor the left leg. of the triangle (63.5º) to the X intercept of the right leg of the triangle (164.6°) and is 101.1°. The left leg of the triangle was obtained from a least-squares fit of the 9 data points between and including points A and B. The right leg of the triangle was obtained from a least-squares fit of the 7 data points between and including points C and D. The magnitude of the background firing rate (6.26 AP/sec) is indicated by the horizontal dotted line. The background firing rate was taken as the mean firing rate for all data points more than 18º counterclockwise from the X intercept of the left leg of the triangle and more than 18° clockwise from the X intercept of the right leg of the triangle (in this case, 39 points). The asymmetry of the triangle was defined as the absolute value of the left leg slope divided by the right leg slope.CC-BY-NC-SA · From the PDF
Figure 5 Histogram of the signal-to-noise ratio of head-direction cell firing. The signal is defined to be the observed peak firing rate. Note that the X axis is plotted on a logarithmic scale.
Figure 5 Histogram of the signal-to-noise ratio of head-direction cell firing. The signal is defined to be the observed peak firing rate. Note that the X axis is plotted on a logarithmic scale.CC-BY-NC-SA · From the PDF
Figure 6 Histograms showing the distribution of peak firing rates for head-direction cells. A, Peak firing rates based on observed values. B, Peak firing rates rates based on observed values. B, Peak firing rates based on the triangular model.
Figure 6 Histograms showing the distribution of peak firing rates for head-direction cells. A, Peak firing rates based on observed values. B, Peak firing rates rates based on observed values. B, Peak firing rates based on the triangular model.CC-BY-NC-SA · From the PDF
Image 8
CC-BY-NC-SA · From the PDF
Figure 7 Histogram showing the distribution of the preferred firing direction for head-direction cells. From the histogram and the statistical analysis described in the text, there was no trend for preferred directions to occur at particular head directions.
Figure 7 Histogram showing the distribution of the preferred firing direction for head-direction cells. From the histogram and the statistical analysis described in the text, there was no trend for preferred directions to occur at particular head directions.CC-BY-NC-SA · From the PDF
Figure 8 Histogram of the directional firing range of head-direction cells. Most cells clustered around a firing range of 90°.
Figure 8 Histogram of the directional firing range of head-direction cells. Most cells clustered around a firing range of 90°.CC-BY-NC-SA · From the PDF
Figure 9 Scattergram of the relationship between directional firing range and peak firing rate for 24 directional cells. The solid line shows the least-squares best-fit of the data (r = +0.516).
Figure 9 Scattergram of the relationship between directional firing range and peak firing rate for 24 directional cells. The solid line shows the least-squares best-fit of the data (r = +0.516).CC-BY-NC-SA · From the PDF
Figure 10 Firing rate as a function of location for 3 head-direction cells. A, The cylinder was divided into 12 equal area sections (3 annuli by 4 quadrants). The firing-rate/head-direction functions for the 12 sections are shown superimposed on each other for the 3 head-direction cells depicted in Figure 3. B, Low-peak-firing-rate cell. C, Medium-peak-firing-rate cell. D, Highpeak-firing-rate cell. In order to avoid undersampling, head directions were analyzed according to 18° bin widths, instead of 6° bin widths used in Figure 3. The results show that for each headdirection cell the rate-direction functions were similar for the 12 sections.
Figure 10 Firing rate as a function of location for 3 head-direction cells. A, The cylinder was divided into 12 equal area sections (3 annuli by 4 quadrants). The firing-rate/head-direction functions for the 12 sections are shown superimposed on each other for the 3 head-direction cells depicted in Figure 3. B, Low-peak-firing-rate cell. C, Medium-peak-firing-rate cell. D, Highpeak-firing-rate cell. In order to avoid undersampling, head directions were analyzed according to 18° bin widths, instead of 6° bin widths used in Figure 3. The results show that for each headdirection cell the rate-direction functions were similar for the 12 sections.CC-BY-NC-SA · From the PDF
Image 13
CC-BY-NC-SA · From the PDF
Image 14
CC-BY-NC-SA · From the PDF
Image 15
CC-BY-NC-SA · From the PDF
Image 16
CC-BY-NC-SA · From the PDF
Image 17
CC-BY-NC-SA · From the PDF
Image 18
CC-BY-NC-SA · From the PDF
Figure 12 Histograms of the firing rates of 3 head-direction cells during ½th-sec episodes during which the head continuously pointed in the preferred direction. A and B, Histograms for 2-directional cells that consistently fired whenever the head was pointed in the preferred direction. C, Histogram for a directional cell that fired irregularly at the preferred direction; this cell fired at high rates (> 18 spikes/sec) for some periods, but discharged at very low rates (0–6 spikes/sec) during other periods.
Figure 12 Histograms of the firing rates of 3 head-direction cells during ½th-sec episodes during which the head continuously pointed in the preferred direction. A and B, Histograms for 2-directional cells that consistently fired whenever the head was pointed in the preferred direction. C, Histogram for a directional cell that fired irregularly at the preferred direction; this cell fired at high rates (> 18 spikes/sec) for some periods, but discharged at very low rates (0–6 spikes/sec) during other periods.CC-BY-NC-SA · From the PDF
Figure 13 Stability of head-direction cell firing across time. Firingrate/head-direction functions for one head-direction cell recorded on 2 occasions 15 d apart. The solid line shows the results for an initial 8-min recording session, while the broken line shows the results for a second 8-min session recorded 15 days later.
Figure 13 Stability of head-direction cell firing across time. Firingrate/head-direction functions for one head-direction cell recorded on 2 occasions 15 d apart. The solid line shows the results for an initial 8-min recording session, while the broken line shows the results for a second 8-min session recorded 15 days later.CC-BY-NC-SA · From the PDF

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Citations

Cites

Research works printed but not linked: 2

  1. O'Keefe, J., and L. Nadel (1978) The Hippocampus as a Cognitive Map, Clarendon, Oxford, U.K.
  2. Ranck, J. B., Jr. (1975) Behavioral correlates and firing repertoires of neurons in dorsal hippocampal formation and septum of unrestrained rats. In The Hippocampus Vol. 2: Neurophysiology and Behavior, R. L. Isaacson and K. H. Pribram, eds., pp. 207-244, Plenum, New York.

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Metadata

Authors
Taube, J., Muller, R., & Ranck, J.
Affiliations
SUNY Downstate Health Sciences University (US)
Venue
The Journal of Neuroscience
Publisher
Society for Neuroscience
Published
1990-02-01
Volume
10
Issue
2
Pages
420-435
ISSN
  • 0270-6474 (ISSN-L)
  • 1529-2401
DOI
10.1523/jneurosci.10-02-00420.1990
PMC
PMC6570151
OpenAlex
W2167403166
Cited by
1,809
References
3
Citations by year
2026: 64 · 2025: 99 · 2024: 120 · 2023: 85 · 2022: 95 · 2021: 83 · 2020: 89 · 2019: 84 · 2018: 97 · 2017: 77 · 2016: 56 · 2015: 78 · 2014: 75 · 2013: 52 · 2012: 45
FWCI
6.48
Type
journal article
Language
en
Open access
Licence
Locations
  • Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
  • Europe PMC (PubMed Central) (publishedVersion)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
Funders
  • National Institutes of Health (5t32ns007117-13, 5r01ns014497-16, 20686)
  • National Institute of Neurological Disorders and Stroke (NS14497, NS07117, NS 20686, R01NS020686)
Topics
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
  • Social Sciences › Psychology › Experimental and Cognitive Psychology › Spatial Cognition and Navigation
  • Life Sciences › Neuroscience › Neurology › Vestibular and auditory disorders
Keywords
head direction cells, postsubiculum, spatial firing patterns, firing rate, freely moving rats, head tracking, hippocampal formation
MeSH terms
Animals, Electrophysiology, Female, Head, Hippocampus, Neurons, Orientation, Rats, Inbred Strains, Time Factors, Rats

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