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Research Articles, Systems/Circuits

A Direct Comparison of Theta Power and Frequency to Speed and Acceleration

Jack P. Kennedy, Yuchen Zhou, Y. Qin, Sarah D. Lovett, A. Sheremet, S. N. Burke and A. P. Maurer
Journal of Neuroscience 25 May 2022, 42 (21) 4326-4341; DOI: https://doi.org/10.1523/JNEUROSCI.0987-21.2022
Jack P. Kennedy
1Department of Neuroscience, McKnight Brain Institute, College of Medicine, University of Florida, Gainesville, Florida 32610
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Yuchen Zhou
2Engineering School of Sustainable Infrastructure & Environment (ESSIE), University of Florida, Gainesville, Florida 32611
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Y. Qin
2Engineering School of Sustainable Infrastructure & Environment (ESSIE), University of Florida, Gainesville, Florida 32611
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Sarah D. Lovett
1Department of Neuroscience, McKnight Brain Institute, College of Medicine, University of Florida, Gainesville, Florida 32610
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A. Sheremet
1Department of Neuroscience, McKnight Brain Institute, College of Medicine, University of Florida, Gainesville, Florida 32610
2Engineering School of Sustainable Infrastructure & Environment (ESSIE), University of Florida, Gainesville, Florida 32611
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S. N. Burke
1Department of Neuroscience, McKnight Brain Institute, College of Medicine, University of Florida, Gainesville, Florida 32610
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A. P. Maurer
1Department of Neuroscience, McKnight Brain Institute, College of Medicine, University of Florida, Gainesville, Florida 32610
2Engineering School of Sustainable Infrastructure & Environment (ESSIE), University of Florida, Gainesville, Florida 32611
3Department of Biomedical Engineering, University of Florida, Gainesville, Florida 32611
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Abstract

Decades of hippocampal neurophysiology research have linked the hippocampal theta rhythm to voluntary movement. A consistent observation has been a robust correlation between the amplitude (or power) and frequency of hippocampal theta and running speed. Recently, however, it has been suggested that acceleration, not running speed, is the dominating influence on theta frequency. There is an inherent interdependence among these two variables, as acceleration is the rate of change in velocity. Therefore, we investigated theta frequency and amplitude of the local-field potential recorded from the stratum pyramidale, stratum radiatum, and stratum lacunosum moleculare of the CA1 subregion, considering both speed and acceleration in tandem as animals traversed a circular task or performed continuous alternation. In male and female rats volitionally controlling their own running characteristics, we found that running speed carries nearly all of the variability in theta frequency and power, with a minute contribution from acceleration. These results contradicted a recent publication using a speed-clamping task, where acceleration and movement are compelled through the use of a bottomless car (Kropff et al., 2021a). Therefore, we reanalyzed the speed-clamping data replicating a transient increase in theta frequency during acceleration. Compared with track running rats, the speed-clamped animals exhibited lower velocities and acceleration values but still showed a stronger influence of speed on theta frequency relative to acceleration. As navigation is the integration of many sensory inputs that are not necessarily linearly related, we offer caution in making absolute claims regarding hippocampal physiology from correlates garnered from a single behavioral repertoire.

SIGNIFICANCE STATEMENT A long-standing, replicable observation has been the increase of hippocampal theta power and frequency with increasing running speed. Recently, however, an experimental approach that clamps the running speed of an animal has suggested that acceleration is the dominant influence. Therefore, we analyzed data from freely behaving rats as well as data from the speed-clamping experiment. In unrestrained behavior, speed remains the dominant behavioral correlate to theta amplitude and frequency. Positive acceleration in the speed-clamp experiment induced a transient increase in theta frequency and power. However, speed retained the dominant influence over theta frequency, changing with velocity in both acceleration and deceleration conditions.

  • hippocampus
  • LFP
  • oscillation
  • rat
  • theta
  • vestibular system

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The Journal of Neuroscience: 42 (21)
Journal of Neuroscience
Vol. 42, Issue 21
25 May 2022
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A Direct Comparison of Theta Power and Frequency to Speed and Acceleration
Jack P. Kennedy, Yuchen Zhou, Y. Qin, Sarah D. Lovett, A. Sheremet, S. N. Burke, A. P. Maurer
Journal of Neuroscience 25 May 2022, 42 (21) 4326-4341; DOI: 10.1523/JNEUROSCI.0987-21.2022

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A Direct Comparison of Theta Power and Frequency to Speed and Acceleration
Jack P. Kennedy, Yuchen Zhou, Y. Qin, Sarah D. Lovett, A. Sheremet, S. N. Burke, A. P. Maurer
Journal of Neuroscience 25 May 2022, 42 (21) 4326-4341; DOI: 10.1523/JNEUROSCI.0987-21.2022
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Keywords

  • hippocampus
  • LFP
  • oscillation
  • rat
  • theta
  • vestibular system

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