Abstract

The integration of muscle cells with soft robotics in recent years has led to the development of biohybrid machines capable of untethered locomotion. A major frontier that currently remains unexplored is neuronal actuation and control of such muscle-powered biohybrid machines. As a step toward this goal, we present here a biohybrid swimmer driven by on-board neuromuscular units. The body of the swimmer consists of a free-standing soft scaffold, skeletal muscle tissue, and optogenetic stem cell-derived neural cluster containing motor neurons. Myoblasts embedded in extracellular matrix self-organize into a muscle tissue guided by the geometry of the scaffold, and the resulting muscle tissue is cocultured in situ with a neural cluster. Motor neurons then extend neurites selectively toward the muscle and innervate it, developing functional neuromuscular units. Based on this initial construct, we computationally designed, optimized, and implemented light-sensitive flagellar swimmers actuated by these neuromuscular units. Cyclic muscle contractions, induced by neural stimulation, drive time-irreversible flagellar dynamics, thereby providing thrust for untethered forward locomotion of the swimmer. Overall, this work demonstrates an example of a biohybrid robot implementing neuromuscular actuation and illustrates a path toward the forward design and control of neuron-enabled biohybrid machines.

Original languageEnglish (US)
Pages (from-to)19841-19847
Number of pages7
JournalProceedings of the National Academy of Sciences of the United States of America
Volume116
Issue number40
Early online dateSep 16 2019
DOIs
StatePublished - Oct 1 2019

Fingerprint

Muscles
Motor Neurons
Locomotion
Optogenetics
Neural Stem Cells
Myoblasts
Robotics
Neurites
Muscle Contraction
Muscle Cells
Extracellular Matrix
Skeletal Muscle
Neurons
Light

Keywords

  • Bioactuator
  • Biohybrid system
  • Neuromuscular junction
  • Swimmer

ASJC Scopus subject areas

  • General

Cite this

Neuromuscular actuation of biohybrid motile bots. / Aydin, Onur; Zhang, Xiaotian; Nuethong, Sittinon; Pagan-Diaz, Gelson J.; Bashir, Rashid; Gazzola, Mattia; Saif, M Taher A.

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 116, No. 40, 01.10.2019, p. 19841-19847.

Research output: Contribution to journalArticle

Aydin, Onur ; Zhang, Xiaotian ; Nuethong, Sittinon ; Pagan-Diaz, Gelson J. ; Bashir, Rashid ; Gazzola, Mattia ; Saif, M Taher A. / Neuromuscular actuation of biohybrid motile bots. In: Proceedings of the National Academy of Sciences of the United States of America. 2019 ; Vol. 116, No. 40. pp. 19841-19847.
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