Beta-frequency sensory stimulation enhances gait rhythmicity through strengthened coupling between striatal networks and stepping movement

• Published in: Nature communications Vol. 15; no. 1; pp. 8336 - 17
• Main Authors: Sridhar, Sudiksha, Lowet, Eric, Gritton, Howard J., Freire, Jennifer, Zhou, Chengqian, Liang, Florence, Han, Xue
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 27.09.2024; Nature Publishing Group; Nature Portfolio
• Subjects: 14; 631/378/2629; 631/378/2632; Acoustic Stimulation; Animals; Beta Rhythm - physiology; Calcium signalling; Corpus Striatum - physiology; Coupling; Delta Rhythm - physiology; Gait; Gait - physiology; Humanities and Social Sciences; Information processing; Locomotion; Locomotion - physiology; Male; Mice; Mice, Inbred C57BL; multidisciplinary; Neostriatum; Nerve Net - physiology; Oscillations; Photic Stimulation; Recording sessions; Rhythm; Rhythms; Science; Science (multidisciplinary); Sensorimotor system; Sensory integration; Sensory stimulation; Synchronization; Translation
• ISSN: 2041-1723; 2041-1723
• DOI: 10.1038/s41467-024-52664-0

Stepping movement is delta (1–4 Hz) rhythmic and depends on sensory inputs. Stepping-related delta-rhythmic neural activity is coupled to beta (10–30 Hz) frequency dynamics that are also prominent in sensorimotor circuits. We explored how beta-frequency sensory stimulation influences stepping and dorsal striatal regulation of stepping. We delivered audiovisual stimulation at 10 or 145 Hz to mice voluntarily locomoting, while recording locomotion, cellular calcium dynamics and local field potentials (LFPs). We found that 10 Hz, but not 145 Hz stimulation prominently entrained striatal LFPs. Even though stimulation at both frequencies promoted locomotion and desynchronized striatal network, only 10 Hz stimulation enhanced the delta rhythmicity of stepping and strengthened the coupling between stepping and striatal LFP delta and beta oscillations. These results demonstrate that higher frequency sensory stimulation can modulate lower frequency striatal neural dynamics and improve stepping rhythmicity, highlighting the translational potential of non-invasive beta-frequency sensory stimulation for improving gait. Whether and how sensory stimulation at beta frequencies could boost motor circuit processing of stepping movement without producing exaggerated beta oscillations are not fully understood. Here authors show that beta frequency audiovisual stimulation enhances stepping rhythmicity via improved striatal regulation of movement in mice, highlighting the translational potential of sensory stimulation in improving gait rhythmicity.