Tags

Type your tag names separated by a space and hit enter

Feedback Signal from Motoneurons Influences a Rhythmic Pattern Generator.
J Neurosci 2017; 37(38):9149-9159JN

Abstract

Motoneurons are not mere output units of neuronal circuits that control motor behavior but participate in pattern generation. Research on the circuit that controls the crawling motor behavior in leeches indicated that motoneurons participate as modulators of this rhythmic motor pattern. Crawling results from successive bouts of elongation and contraction of the whole leech body. In the isolated segmental ganglia, dopamine can induce a rhythmic antiphasic activity of the motoneurons that control contraction (DE-3 motoneurons) and elongation (CV motoneurons). The study was performed in isolated ganglia where manipulation of the activity of specific motoneurons was performed in the course of fictive crawling (crawling). In this study, the membrane potential of CV was manipulated while crawling was monitored through the rhythmic activity of DE-3. Matching behavioral observations that show that elongation dominates the rhythmic pattern, the electrophysiological activity of CV motoneurons dominates the cycle. Brief excitation of CV motoneurons during crawling episodes resets the rhythmic activity of DE-3, indicating that CV feeds back to the rhythmic pattern generator. CV hyperpolarization accelerated the rhythm to an extent that depended on the magnitude of the cycle period, suggesting that CV exerted a positive feedback on the unit(s) of the pattern generator that controls the elongation phase. A simple computational model was implemented to test the consequences of such feedback. The simulations indicate that the duty cycle of CV depended on the strength of the positive feedback between CV and the pattern generator circuit.SIGNIFICANCE STATEMENT Rhythmic movements of animals are controlled by neuronal networks that have been conceived as hierarchical structures. At the basis of this hierarchy, we find the motoneurons, few neurons at the top control global aspects of the behavior (e.g., onset, duration); and within these two ends, specific neuronal circuits control the actual rhythmic pattern of movements. We have investigated whether motoneurons are limited to function as output units. Analysis of the network that controls crawling behavior in the leech has clearly indicated that motoneurons, in addition to controlling muscle activity, send signals to the pattern generator. Physiological and modeling studies on the role of specific motoneurons suggest that these feedback signals modulate the phase relationship of the rhythmic activity.

Authors+Show Affiliations

Department of Mathematical Sciences, New Jersey Institute of Technology, University Heights, Newark, New Jersey 07102.Departamento de Fisiología, Biología Molecular y Celular Dr. Héctor Maldonado, Universidad de Buenos Aires, Facultad de Ciencias Exactas y Naturales, and. Instituto de Fisiología, Biología Molecular y Neurociencias, CONICET-Universidad de Buenos Aires, 1428 Buenos Aires, Argentina.Departamento de Fisiología, Biología Molecular y Celular Dr. Héctor Maldonado, Universidad de Buenos Aires, Facultad de Ciencias Exactas y Naturales, and szczupak@retina.ar. Instituto de Fisiología, Biología Molecular y Neurociencias, CONICET-Universidad de Buenos Aires, 1428 Buenos Aires, Argentina.

Pub Type(s)

Journal Article
Research Support, Non-U.S. Gov't

Language

eng

PubMed ID

28821650

Citation

Rotstein, Horacio G., et al. "Feedback Signal From Motoneurons Influences a Rhythmic Pattern Generator." The Journal of Neuroscience : the Official Journal of the Society for Neuroscience, vol. 37, no. 38, 2017, pp. 9149-9159.
Rotstein HG, Schneider E, Szczupak L. Feedback Signal from Motoneurons Influences a Rhythmic Pattern Generator. J Neurosci. 2017;37(38):9149-9159.
Rotstein, H. G., Schneider, E., & Szczupak, L. (2017). Feedback Signal from Motoneurons Influences a Rhythmic Pattern Generator. The Journal of Neuroscience : the Official Journal of the Society for Neuroscience, 37(38), pp. 9149-9159. doi:10.1523/JNEUROSCI.0756-17.2017.
Rotstein HG, Schneider E, Szczupak L. Feedback Signal From Motoneurons Influences a Rhythmic Pattern Generator. J Neurosci. 2017 09 20;37(38):9149-9159. PubMed PMID: 28821650.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Feedback Signal from Motoneurons Influences a Rhythmic Pattern Generator. AU - Rotstein,Horacio G, AU - Schneider,Elisa, AU - Szczupak,Lidia, Y1 - 2017/08/16/ PY - 2017/03/13/received PY - 2017/08/01/revised PY - 2017/08/09/accepted PY - 2017/8/20/pubmed PY - 2017/10/5/medline PY - 2017/8/20/entrez KW - Morris–Lecar model KW - duty cycle KW - dye coupling KW - leech crawling KW - left-right symmetry KW - phase relationship SP - 9149 EP - 9159 JF - The Journal of neuroscience : the official journal of the Society for Neuroscience JO - J. Neurosci. VL - 37 IS - 38 N2 - Motoneurons are not mere output units of neuronal circuits that control motor behavior but participate in pattern generation. Research on the circuit that controls the crawling motor behavior in leeches indicated that motoneurons participate as modulators of this rhythmic motor pattern. Crawling results from successive bouts of elongation and contraction of the whole leech body. In the isolated segmental ganglia, dopamine can induce a rhythmic antiphasic activity of the motoneurons that control contraction (DE-3 motoneurons) and elongation (CV motoneurons). The study was performed in isolated ganglia where manipulation of the activity of specific motoneurons was performed in the course of fictive crawling (crawling). In this study, the membrane potential of CV was manipulated while crawling was monitored through the rhythmic activity of DE-3. Matching behavioral observations that show that elongation dominates the rhythmic pattern, the electrophysiological activity of CV motoneurons dominates the cycle. Brief excitation of CV motoneurons during crawling episodes resets the rhythmic activity of DE-3, indicating that CV feeds back to the rhythmic pattern generator. CV hyperpolarization accelerated the rhythm to an extent that depended on the magnitude of the cycle period, suggesting that CV exerted a positive feedback on the unit(s) of the pattern generator that controls the elongation phase. A simple computational model was implemented to test the consequences of such feedback. The simulations indicate that the duty cycle of CV depended on the strength of the positive feedback between CV and the pattern generator circuit.SIGNIFICANCE STATEMENT Rhythmic movements of animals are controlled by neuronal networks that have been conceived as hierarchical structures. At the basis of this hierarchy, we find the motoneurons, few neurons at the top control global aspects of the behavior (e.g., onset, duration); and within these two ends, specific neuronal circuits control the actual rhythmic pattern of movements. We have investigated whether motoneurons are limited to function as output units. Analysis of the network that controls crawling behavior in the leech has clearly indicated that motoneurons, in addition to controlling muscle activity, send signals to the pattern generator. Physiological and modeling studies on the role of specific motoneurons suggest that these feedback signals modulate the phase relationship of the rhythmic activity. SN - 1529-2401 UR - https://www.unboundmedicine.com/medline/citation/28821650/Feedback_Signal_from_Motoneurons_Influences_a_Rhythmic_Pattern_Generator_ L2 - http://www.jneurosci.org/cgi/pmidlookup?view=long&pmid=28821650 DB - PRIME DP - Unbound Medicine ER -