HIPPOCAMPAL THETA OSCILLATIONS DURING CONTROLLED SPEED RUNS ON A TREADMILL

Abstract

Hippocampal theta (6-12 Hz) oscillations coordinate neural activity during spatial navigation and are strongly related to locomotion speed. However, recent research has yielded conflicting evidence on whether theta rhythms are primarily modulated by acceleration or instantaneous speed. Moreover, the role of movement transitions--at locomotion onset and offset--has often been overlooked, despite potentially involving distinct dynamics not explained by speed or acceleration alone. Previous studies have rarely controlled for locomotion timing and speed, limiting our ability to dissociate the contributions of speed, acceleration, and movement transitions. To address this, we used a computer-controlled treadmill to induce rat locomotion under three distinct conditions: (a) movement transitions, (b) steady running at constant speed, and (c) locomotion with continuous acceleration. This setup allowed precise spectral analysis of hippocampal theta oscillations across conditions. We found that treadmill-triggered movement transitions produced sustained increases in theta power and transient increases in theta frequency. Upon treadmill stop, theta power decreased slowly, whereas theta frequency dropped rapidly. Steady running elevated both theta power and frequency relative to rest. During constant-speed trials, both metrics increased with speed and remained stable over time. Notably, the acceleration rate itself had no effect on theta power or frequency. Instead, during accelerating trials, theta frequency increased progressively with instantaneous speed, underscoring speed as the primary modulator. In summary, our results show that movement transitions induce distinct, sustained changes in theta power and transient changes in theta frequency, while instantaneous speed--not acceleration--governs hippocampal theta frequency. Significance statementThe precise contributions of movement transitions, speed, and acceleration to hippocampal theta oscillations remain unclear due to confounding factors in freely moving paradigms. To resolve this, we employed a computer-controlled treadmill to systematically isolate each locomotor variable under tightly controlled conditions. Our results demonstrate that movement transitions induce distinct changes in theta power and frequency, and that instantaneous speed--not acceleration--robustly modulates theta frequency across hippocampal subregions. These findings clarify an ongoing debate and refine our understanding of how specific locomotor dynamics shape hippocampal activity during navigation.