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ARTICLE, Behavioral/Systems

Neural Correlates for Angular Head Velocity in the Rat Dorsal Tegmental Nucleus

Joshua P. Bassett and Jeffrey S. Taube
Journal of Neuroscience 1 August 2001, 21 (15) 5740-5751; DOI: https://doi.org/10.1523/JNEUROSCI.21-15-05740.2001
Joshua P. Bassett
1Department of Psychological and Brain Sciences, Center for Cognitive Neuroscience, Dartmouth College, Hanover, New Hampshire 03755
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Jeffrey S. Taube
1Department of Psychological and Brain Sciences, Center for Cognitive Neuroscience, Dartmouth College, Hanover, New Hampshire 03755
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  • Fig. 1.
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    Fig. 1.

    A, Schematic illustration of a coronal section showing DTN at −9.16 mm posterior to bregma. The DTN are shaded bilaterally. B, Photomicrograph of a coronal section stained with cresyl violet. Two electrode tracks are visible passing through the DTN in the left hemisphere; a white arrow points to the center of the intact DTN in the right hemisphere [modified from Paxinos and Watson (1998)]. 4V, Fourth ventricle; Cb, cerebellum; LC, locus coeruleus; mcp, middle cerebellar peduncle; Me5, mesencephalic nucleus of V; ml, medial lemniscus; mlf, medial longitudinal fasciculus; PaS, parasubiculum;py, pyramidal tract; rs, rubrospinal tract; scp, superior cerebellar peduncle;tz, trapezoid body; Tz, nucleus of the trapezoid body. Scale bar, 250 μm.

  • Fig. 2.
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    Fig. 2.

    Symmetric AHV cells. Examples of different symmetric AHV cells showing different variations of the firing rate by AHV functions. A, AHV cell showing linear functions from low to high AHVs. B, Cell with steep slopes at low AHVs and shallower slopes above ∼90°/sec. C, Cell with steep slopes at low AHVs and near-zero slopes at high AHVs. CW and CCW directions are as indicated in A for all graphs.

  • Fig. 3.
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    Fig. 3.

    A, Frequency distribution histogram of the slopes of the firing rate–AHV function for symmetric AHV cells. A wide range of slope values is displayed across all cells.B, Firing rate at 45°/sec as a percentage of the maximum firing rate for symmetric AHV cells. Cells approach their peak firing rates across a wide range of AHVs. Consequently, there is a wide range of percentages observed across the AHV cell population, suggesting that each cell is tuned to maximally encode a specific AHV range.

  • Fig. 4.
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    Fig. 4.

    Asymmetric AHV cells. Examples of different asymmetric AHV cells showing different variations of the firing rate by AHV functions. A, A frequently observed pattern of symmetric modulation at low AHVs around 0°/sec that changes to an asymmetric pattern at higher velocities. B, A linear increase in firing rate in the preferred turn direction but no modulation of firing rate in the nonpreferred turn direction.C, An atypical cell in which the firing rate was negatively correlated with AHV during CCW head turns but was not correlated at all with AHV during CW head turns. CW and CCW directions are as indicated in A for all graphs.

  • Fig. 5.
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    Fig. 5.

    Autocorrelograms from symmetric (A) and asymmetric (B) AHV cells with irregular firing patterns. Both graphs were constructed from head turns of ≤6°/sec, reflecting the tonic resting rate of the cell. For both A and B, the 1 msec bin centered around 0 (−0.5 to +0.5 msec) contains zero spikes; the corresponding empty bins are obscured by the small time scale.

  • Fig. 6.
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    Fig. 6.

    Firing rate and dwell time as a function of HD.A, B, Each solid line indicates the firing rate, and each dashed line indicates the time spent in each directional bin (in samples that are 1/60th of a second). In neither case is there any relationship between firing rate and dwell time, but in A, firing rate is elevated throughout a wide range of HDs centered on ∼100°.

  • Fig. 7.
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    Fig. 7.

    Firing rate as a function of HD in different AHV ranges. Firing rate by HD functions were determined separately for samples obtained during head turns of 0–90, 90–180, or 180–1000°/sec. The firing rate is elevated at high AHVs at all HDs, but by a greater margin in the directional firing range. The firing rate by HD function for head turns between 90 and 180°/sec is omitted for the sake of clarity, but this function was situated approximately between the other two functions.

  • Fig. 8.
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    Fig. 8.

    Two examples of DTN AHV cells that were also modulated by the animal's head pitch. The left columnshows the firing rate versus head pitch plots. The plots in theright column show the firing rate versus AHV functions for the same cells. A, Symmetric AHV cell.B, Asymmetric AHV cell. Head pitch values >40° are considered free of contamination from negative head pitches. CW and CCW directions are as indicated in Figure 2 for all AHV graphs.

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    Fig. 9.

    LMN AHV cells. Firing rate versus AHV plots for different types of AHV cells in LMN are shown. A, Symmetric. B, Asymmetric. C, Example of a cell that was considered previously to be modulated by AHV (Stackman and Taube, 1998) but that was excluded from the present analysis because its modulation was considered too weak. CW and CCW directions are as indicated in A for all graphs.

  • Fig. 10.
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    Fig. 10.

    Summary of the connections between different brain areas involved in the HD cell network and model of how DTN symmetric and asymmetric AHV cells may be connected to generate and update the LMN HD cell signal. The example shown is for the left hemisphere and a CW head turn. The connectivity in the right hemisphere would be similar, except that the right DTN would contain mostly CCW asymmetric AHV cells. Shaded areas process primarily AHV information; unshaded areas process primarily HD information. HD units depict directional “modules” of cell groups; each unit signals different directional headings. Tonic excitation of HD cells when the head is not moving may be the result of HD feedback from the postsubiculum, intrinsic membrane properties, or still undiscovered excitatory projections into LMN. Lateral inhibition of HD cells outside the current directional heading is accomplished via tonic firing from inhibitory DTN AHV cells that are modulated by HD (Fig. 6) and perhaps similarly via LMN AHV cells. An HD cell signaling the current heading could further enhance lateral inhibition by suppressing tonic inhibition of itself via inhibitory interneurons in the DTN (shown by the asterisk). During a CW head turn, excitatory projections from nPH outweigh feedback inhibition on AHV cells in the DTN. The burst of activity in CW asymmetric AHV cells in the DTN (which are more abundant in the left hemisphere) forces the HD activity hill CW. The HD cell on the CW side of the activity hill is disinhibited because of asymmetric, offset connectivity, in which an HD cell tuned to 0° is inhibited by a CW asymmetric AHV cell tuned to −10°. Projections from the contralateral DTN (data not shown) may play a role in offsetting this asymmetry, because LMN HD cells fire in both head turn directions. They may also augment or take the place of type I afferents from nPH. During CCW head turns, asymmetric AHV cells in the right hemisphere that have a CCW preferred turn direction (data not shown) initiate the shift of the activity hill.ASYM, Asymmetric; HD, head direction cell;SYMM, symmetric.

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    Table 1.

    Firing parameters of DTN and LMN AHV cells

    DTN symmetricLMN symmetricDTN asymmetricLMN asymmetric
    Number/total22/4413/3011/448/30
    AHV correlation coefficient (r)0.605  ± 0.0590.435  ± 0.1190.538  ± 0.0770.446  ± 0.126
    Linear velocity correlation (r)0.289  ± 0.0290.165  ± 0.048*0.146  ± 0.0630.027  ± 0.064
    Slope (spikes per degree per second)0.0443  ± 0.00340.0144  ± 0.0061*0.0318  ± 0.01130.0275  ± 0.0106
    Baseline firing rate (spikes/sec)8.7  ± 1.07.6  ± 1.95.6  ± 1.318.3  ± 5.3*
    Peak firing rate (spikes/sec)27.7  ± 2.214.2  ± 4.019.1  ± 6.227.8  ± 5.7
    • ↵* Significantly different from DTN, p < 0.05.

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The Journal of Neuroscience: 21 (15)
Journal of Neuroscience
Vol. 21, Issue 15
1 Aug 2001
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Neural Correlates for Angular Head Velocity in the Rat Dorsal Tegmental Nucleus
Joshua P. Bassett, Jeffrey S. Taube
Journal of Neuroscience 1 August 2001, 21 (15) 5740-5751; DOI: 10.1523/JNEUROSCI.21-15-05740.2001

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Neural Correlates for Angular Head Velocity in the Rat Dorsal Tegmental Nucleus
Joshua P. Bassett, Jeffrey S. Taube
Journal of Neuroscience 1 August 2001, 21 (15) 5740-5751; DOI: 10.1523/JNEUROSCI.21-15-05740.2001
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Keywords

  • dorsal tegmental nucleus of Gudden
  • lateral mammillary nuclei
  • head direction cell
  • angular head velocity
  • nucleus prepositus hypoglossi
  • directional heading
  • neural integration
  • vestibular system
  • navigation
  • spatial orientation

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