Ultrasound Stimulations Induce Prolonged Depolarization and Fast Action Potentials in Leech Neurons

Francesca Dedola; Francesco Paolo Ulloa Severino; Nicolo Meneghetti; Theo Lemaire; Andrea Cafarelli; Leonardo Ricotti; Arianna Menciassi; Annarita Cutrone; Alberto Mazzoni; Silvestro Micera

doi:10.1109/OJEMB.2019.2963474

Ultrasound Stimulations Induce Prolonged Depolarization and Fast Action Potentials in Leech Neurons

IEEE Open J Eng Med Biol. 2020 Feb 14:1:23-32. doi: 10.1109/OJEMB.2019.2963474. eCollection 2020.

Authors

Francesca Dedola^{1

2}, Francesco Paolo Ulloa Severino³, Nicolo Meneghetti^{1

2}, Theo Lemaire⁴, Andrea Cafarelli^{1

2}, Leonardo Ricotti^{1

2}, Arianna Menciassi^{1

2}, Annarita Cutrone^{1

2}, Alberto Mazzoni^{1

2}, Silvestro Micera^{5

2

6}

Affiliations

¹ 1 The Biorobotics InstituteScuola Superiore Sant'Anna Pisa 56025 Italy.
² Department of Excellence in Robotics and AIScuola Superiore Sant'Anna Pisa 56025 Italy.
³ 2 Neuroscience AreaInternational School for Advanced Studies Trietse 341356 Italy.
⁴ 3 Bertarelli Foundation Chair in Translational NeuroEngineering, Center for Neuroprosthetics and Institute of BioengineeringSchool of Engineering, Ecole Polytechnique Federale de Lausanne Lausanne 1015 Switzerland.
⁵ 4 BioRobotics InstituteScuola Superiore Sant'Anna Pisa 56025 Italy.
⁶ Bertarelli Foundation Chair in Translational NeuroEngineering, Center for Neuroprosthetics and Institute of BioengineeringSchool of Engineering, Ecole Polytechnique Federale de Lausanne Lausanne 1015 Switzerland.

Abstract

Objective: Ultrasound (US) stimulation carries the promise of a selective, reversible, and non-invasive modulation of neural activity without the need for genetic manipulation of neural structures. However, the mechanisms of US-induced generation of action potentials (APs) are still unclear. Methods: Here we address this issue by analyzing intracellularly recorded responses of leech nociceptive neurons to controlled delivery of US. Results: US induced a depolarization linearly accumulating in time and outlasting the duration of the stimulation. Spiking activity was reliably induced for an optimal US intensity range. Moreover, we found that APs induced by US differ in smaller amplitude and faster repolarization from those induced by electrical stimulation in the same cell but display the same repolarization rate. Conclusions: These results shed light on the mechanism by which spikes are induced by US and pave the way for designing more efficient US stimulation patterns.

Keywords: Action Potential; Depolarization; Leech; Neuromodulation; Ultrasounds.

Grants and funding

This study was partly funded by the Bertarelli Foundation, the Wyss Center for Bio- and Neuroengineering, the European Union (project M2NEURAL), by the Italian Ministry of Education, University and Research (MIUR) through the PRIN project PROTECTION, and by the National Competence Center Research (NCCR) Robotics by the Swiss National Science Foundation.