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Hippocampal delta oscillations entrain neuronal activity, modulate gamma amplitude and convey information about running speed on a treadmill

View ORCID ProfileAlan MB Furtunato, View ORCID ProfileRafael Pedrosa, View ORCID ProfileBruno Lobão-Soares, View ORCID ProfileAdriano BL Tort, View ORCID ProfileHindiael Belchior
doi: https://doi.org/10.1101/2022.01.24.477542
Alan MB Furtunato
1Brain Institute, Federal University of Rio Grande do Norte, Natal, RN 59078-970, Brazil
2Psychobiology Graduate Program, Federal University of Rio Grande do Norte, Natal, RN 59078-970, Brazil
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Rafael Pedrosa
1Brain Institute, Federal University of Rio Grande do Norte, Natal, RN 59078-970, Brazil
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Bruno Lobão-Soares
2Psychobiology Graduate Program, Federal University of Rio Grande do Norte, Natal, RN 59078-970, Brazil
3Department of Pharmacology, Federal University of Rio Grande do Norte, Natal, RN 59078-970, Brazil
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Adriano BL Tort
1Brain Institute, Federal University of Rio Grande do Norte, Natal, RN 59078-970, Brazil
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Hindiael Belchior
1Brain Institute, Federal University of Rio Grande do Norte, Natal, RN 59078-970, Brazil
2Psychobiology Graduate Program, Federal University of Rio Grande do Norte, Natal, RN 59078-970, Brazil
4Department of Physical Education, Federal University of Rio Grande do Norte, Natal, RN 59078-970, Brazil
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  • For correspondence: belchior@neuro.ufrn.br
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ABSTRACT

Locomotion has long been associated with rhythmic oscillations in the rat hippocampus. Running speed and acceleration affect the spectral density at the theta (6-10 Hz) and gamma (30-150 Hz) bands and the rhythmic entrainment of neuronal activity. However, less is known about other oscillatory rhythms. Recent studies have shown that oscillatory activity in the delta (1-4 Hz) band also relates to locomotion in stationary conditions, such as running on a treadmill or in a running wheel. To further investigate the effects of stationary running on hippocampal oscillations, we recorded CA1 local field potentials and neuronal activity while rats ran at different speed protocols on a treadmill. We found a remarkable oscillatory activity at 2 Hz that was strongly modulated by running speed. Delta power and peak frequency were highest at the fastest running speed, both in constant and progressively increasing speed protocols. Delta and theta oscillations co-occurred and showed independent relationships in their instantaneous power and frequency. Moreover, the delta phase modulated the amplitude of low-gamma (20-50 Hz) oscillations and the spiking activity of putative pyramidal neurons in a speed-dependent manner. Finally, spectral components in the delta frequency range, but not theta, predicted running speed using a naive Bayes classifier. In summary, our study shows that locomotion-related delta oscillations convey information about stationary running speed and coordinate hippocampal rhythmic activity in a speed-dependent manner.

Statement of significance Theta and gamma oscillations are hallmarks of rhythmic activity in the rat hippocampus during locomotion and exploratory behaviors, but less is known about other oscillatory rhythms. This study shows the emergence of delta (∼2 Hz) oscillations in the dorsal CA1 of rats running on a treadmill. Locomotion-related delta oscillations are independent of the concomitant theta activity and convey information about running speed. Delta waves modulate low-gamma oscillations and the spiking activity of pyramidal neurons in a speed-dependent way. These results suggest that oscillatory activity in the delta band aids rhythmic coordination during stationary locomotor behaviors.

Competing Interest Statement

The authors have declared no competing interest.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted January 25, 2022.
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Hippocampal delta oscillations entrain neuronal activity, modulate gamma amplitude and convey information about running speed on a treadmill
Alan MB Furtunato, Rafael Pedrosa, Bruno Lobão-Soares, Adriano BL Tort, Hindiael Belchior
bioRxiv 2022.01.24.477542; doi: https://doi.org/10.1101/2022.01.24.477542
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Hippocampal delta oscillations entrain neuronal activity, modulate gamma amplitude and convey information about running speed on a treadmill
Alan MB Furtunato, Rafael Pedrosa, Bruno Lobão-Soares, Adriano BL Tort, Hindiael Belchior
bioRxiv 2022.01.24.477542; doi: https://doi.org/10.1101/2022.01.24.477542

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