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Phase-Specific Motor Efference during a Rhythmic Motor Pattern.
J Neurosci. 2020 Feb 26; 40(9):1888-1896.JN

Abstract

Neuronal circuits that control motor behaviors orchestrate multiple tasks, including the inhibition of self-generated sensory signals. In the hermaphroditic leech, T and P mechanosensory neurons respond to light touch and pressure on the skin, respectively. We show that the low threshold T cells were also sensitive to topological changes of the animal surface, caused by contraction of the muscles that erect the skin annuli. P cells were unresponsive to this movement. Annuli erection is part of the contraction phase of crawling, a leech locomotive behavior. In isolated ganglia, T cells showed phase-dependent IPSPs during dopamine-induced fictive crawling, whereas P cells were unaffected. The timing and magnitude of the T-IPSPs were highly correlated with the activity of the motoneurons excited during the contraction phase. Together, the results suggest that the central network responsible for crawling sends a reafferent signal onto the T cells, concomitant with the signal to the motoneurons. This reafference is specifically targeted at the sensory neurons that are affected by the movements; and it is behaviorally relevant as excitation of T cells affected the rhythmic motor pattern, probably acting upon the rhythmogenic circuit. Corollary discharge is a highly conserved function of motor systems throughout evolution, and we provide clear evidence of the specificity of its targets and timing and of the benefit of counteracting self-generated sensory input.SIGNIFICANCE STATEMENT Neuronal circuits that control motor behaviors orchestrate multiple tasks, including inhibition of sensory signals originated by the animal movement, a phenomenon known as corollary discharge. Leeches crawl on solid surfaces through a sequence of elongation and contraction movements. During the contraction, the skin topology changes, affecting a subpopulation of mechanosensory receptors, T (touch) neurons, but not P (pressure) sensory neurons. In the isolated nervous system, T neurons were inhibited during the contraction but not during the elongation phase, whereas P cells were unaffected throughout crawling. Excitation of T cells during the contraction phase temporarily disrupted the rhythmic pattern. Thus, corollary discharge was target (T vs P) and phase (contraction vs elongation) specific, and prevented self-generated signals to perturb motor behaviors.

Authors+Show Affiliations

Departamento de Fisiología, Biología Molecular y Celular, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires and Instituto de Fisiología, Biología Molecular y Neurociencias, Ciudad Universitaria, (C1428EHA) Buenos Aires, Argentina.Departamento de Fisiología, Biología Molecular y Celular, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires and Instituto de Fisiología, Biología Molecular y Neurociencias, Ciudad Universitaria, (C1428EHA) Buenos Aires, Argentina.Departamento de Fisiología, Biología Molecular y Celular, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires and Instituto de Fisiología, Biología Molecular y Neurociencias, Ciudad Universitaria, (C1428EHA) Buenos Aires, Argentina szczupak@retina.ar.

Pub Type(s)

Journal Article

Language

eng

PubMed ID

31980584

Citation

Alonso, Ignacio, et al. "Phase-Specific Motor Efference During a Rhythmic Motor Pattern." The Journal of Neuroscience : the Official Journal of the Society for Neuroscience, vol. 40, no. 9, 2020, pp. 1888-1896.
Alonso I, Sanchez Merlinsky A, Szczupak L. Phase-Specific Motor Efference during a Rhythmic Motor Pattern. J Neurosci. 2020;40(9):1888-1896.
Alonso, I., Sanchez Merlinsky, A., & Szczupak, L. (2020). Phase-Specific Motor Efference during a Rhythmic Motor Pattern. The Journal of Neuroscience : the Official Journal of the Society for Neuroscience, 40(9), 1888-1896. https://doi.org/10.1523/JNEUROSCI.1201-19.2020
Alonso I, Sanchez Merlinsky A, Szczupak L. Phase-Specific Motor Efference During a Rhythmic Motor Pattern. J Neurosci. 2020 Feb 26;40(9):1888-1896. PubMed PMID: 31980584.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Phase-Specific Motor Efference during a Rhythmic Motor Pattern. AU - Alonso,Ignacio, AU - Sanchez Merlinsky,Agustín, AU - Szczupak,Lidia, Y1 - 2020/01/24/ PY - 2019/05/15/received PY - 2020/01/14/revised PY - 2020/01/15/accepted PY - 2020/08/26/pmc-release PY - 2020/1/26/pubmed PY - 2020/1/26/medline PY - 2020/1/26/entrez KW - corollary discharge KW - leech KW - mechanosensory KW - rhythmic motor behaviour SP - 1888 EP - 1896 JF - The Journal of neuroscience : the official journal of the Society for Neuroscience JO - J. Neurosci. VL - 40 IS - 9 N2 - Neuronal circuits that control motor behaviors orchestrate multiple tasks, including the inhibition of self-generated sensory signals. In the hermaphroditic leech, T and P mechanosensory neurons respond to light touch and pressure on the skin, respectively. We show that the low threshold T cells were also sensitive to topological changes of the animal surface, caused by contraction of the muscles that erect the skin annuli. P cells were unresponsive to this movement. Annuli erection is part of the contraction phase of crawling, a leech locomotive behavior. In isolated ganglia, T cells showed phase-dependent IPSPs during dopamine-induced fictive crawling, whereas P cells were unaffected. The timing and magnitude of the T-IPSPs were highly correlated with the activity of the motoneurons excited during the contraction phase. Together, the results suggest that the central network responsible for crawling sends a reafferent signal onto the T cells, concomitant with the signal to the motoneurons. This reafference is specifically targeted at the sensory neurons that are affected by the movements; and it is behaviorally relevant as excitation of T cells affected the rhythmic motor pattern, probably acting upon the rhythmogenic circuit. Corollary discharge is a highly conserved function of motor systems throughout evolution, and we provide clear evidence of the specificity of its targets and timing and of the benefit of counteracting self-generated sensory input.SIGNIFICANCE STATEMENT Neuronal circuits that control motor behaviors orchestrate multiple tasks, including inhibition of sensory signals originated by the animal movement, a phenomenon known as corollary discharge. Leeches crawl on solid surfaces through a sequence of elongation and contraction movements. During the contraction, the skin topology changes, affecting a subpopulation of mechanosensory receptors, T (touch) neurons, but not P (pressure) sensory neurons. In the isolated nervous system, T neurons were inhibited during the contraction but not during the elongation phase, whereas P cells were unaffected throughout crawling. Excitation of T cells during the contraction phase temporarily disrupted the rhythmic pattern. Thus, corollary discharge was target (T vs P) and phase (contraction vs elongation) specific, and prevented self-generated signals to perturb motor behaviors. SN - 1529-2401 UR - https://www.unboundmedicine.com/medline/citation/31980584/Phase-Specific_Motor_Efference_during_a_Rhythmic_Motor_Pattern L2 - http://www.jneurosci.org/cgi/pmidlookup?view=long&pmid=31980584 DB - PRIME DP - Unbound Medicine ER -
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