Literature DB >> 19776260

Distinct inhibitory neurons exert temporally specific control over activity of a motoneuron receiving concurrent excitation and inhibition.

Kosei Sasaki1, Vladimir Brezina, Klaudiusz R Weiss, Jian Jing.   

Abstract

Recent work suggests that concurrent excitation and inhibition originating in central pattern generators (CPGs) may be used to control rhythmic motoneuronal activity. The specific roles that the inhibition plays in such cases are not well understood, however, in part because of the lack of identification of presynaptic inhibitory neurons. Here we demonstrate that, in the Aplysia feeding CPG, inhibitory inputs may be critical for flexible control of the activity of motoneurons in different forms of behavior. The feeding CPG generates ingestive and egestive motor programs, differing in the high and low activity, respectively, of the motoneuron B8 during the retraction phase of the programs. We show that, during retraction, B8 receives concurrent excitation and inhibition that produces a high-conductance state. The inhibition originates in two types of CPG neurons, B4/5 and B70, that are more active in egestion than ingestion and play a role in suppressing B8 activity during egestion. In turn, the activities of both B4/5 and B70 are suppressed by the ingestion-promoting descending interneuron CBI-3 (for cerebral-buccal interneuron 3). Thus, concurrent excitation and inhibition may be an effective means of controlling motoneuronal activity in a behavior-dependent manner. More detailed analyses reveal, furthermore, that B4/5 and B70 exert complementary actions by acting preferentially in the early and late part of retraction, respectively. Thus, the use of multiple neurons to generate inhibitory inputs to motoneurons that receive concurrent excitation and inhibition brings an additional level of flexibility that allows a temporally specific control of motoneuronal activity within a single phase of motor programs.

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Year:  2009        PMID: 19776260      PMCID: PMC2796268          DOI: 10.1523/JNEUROSCI.3051-09.2009

Source DB:  PubMed          Journal:  J Neurosci        ISSN: 0270-6474            Impact factor:   6.167


  57 in total

1.  Concerted GABAergic actions of Aplysia feeding interneurons in motor program specification.

Authors:  Jian Jing; Ferdinand S Vilim; Jin-Sheng Wu; Ji-Ho Park; Klaudiusz R Weiss
Journal:  J Neurosci       Date:  2003-06-15       Impact factor: 6.167

Review 2.  The high-conductance state of neocortical neurons in vivo.

Authors:  Alain Destexhe; Michael Rudolph; Denis Paré
Journal:  Nat Rev Neurosci       Date:  2003-09       Impact factor: 34.870

3.  Frequency-dependent regulation of afferent transmission in the feeding circuitry of Aplysia.

Authors:  Colin G Evans; Jian Jing; Alex Proekt; Steven C Rosen; Elizabeth C Cropper
Journal:  J Neurophysiol       Date:  2003-09-24       Impact factor: 2.714

4.  Dynamical basis of intentions and expectations in a simple neuronal network.

Authors:  Alex Proekt; Vladimir Brezina; Klaudiusz R Weiss
Journal:  Proc Natl Acad Sci U S A       Date:  2004-06-14       Impact factor: 11.205

5.  The construction of movement with behavior-specific and behavior-independent modules.

Authors:  Jian Jing; Elizabeth C Cropper; Itay Hurwitz; Klaudiusz R Weiss
Journal:  J Neurosci       Date:  2004-07-14       Impact factor: 6.167

6.  Dopaminergic contributions to modulatory functions of a dual-transmitter interneuron in Aplysia.

Authors:  Michael R Due; Jian Jing; Klaudiusz R Weiss
Journal:  Neurosci Lett       Date:  2004-03-18       Impact factor: 3.046

7.  Bilateral symmetry and interneuronal organization in the buccal ganglia of Aplysia.

Authors:  D Gardner
Journal:  Science       Date:  1971-08-06       Impact factor: 47.728

8.  Interneuronal basis of the generation of related but distinct motor programs in Aplysia: implications for current neuronal models of vertebrate intralimb coordination.

Authors:  Jian Jing; Klaudiusz R Weiss
Journal:  J Neurosci       Date:  2002-07-15       Impact factor: 6.167

9.  A specific synaptic pathway activates a conditional plateau potential underlying protraction phase in the Aplysia feeding central pattern generator.

Authors:  Nikolai C Dembrow; Jian Jing; Vladimir Brezina; Klaudiusz R Weiss
Journal:  J Neurosci       Date:  2004-06-02       Impact factor: 6.167

10.  Predicting adaptive behavior in the environment from central nervous system dynamics.

Authors:  Alex Proekt; Jane Wong; Yuriy Zhurov; Nataliya Kozlova; Klaudiusz R Weiss; Vladimir Brezina
Journal:  PLoS One       Date:  2008-11-07       Impact factor: 3.240

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  25 in total

Review 1.  Alternation of agonists and antagonists during turtle hindlimb motor rhythms.

Authors:  Paul S G Stein
Journal:  Ann N Y Acad Sci       Date:  2010-06       Impact factor: 5.691

2.  The same core rhythm generator underlies different rhythmic motor patterns.

Authors:  Rachel S White; Michael P Nusbaum
Journal:  J Neurosci       Date:  2011-08-10       Impact factor: 6.167

Review 3.  GABA as a Neurotransmitter in Gastropod Molluscs.

Authors:  Mark W Miller
Journal:  Biol Bull       Date:  2019-01-16       Impact factor: 1.818

4.  Composite modulatory feedforward loop contributes to the establishment of a network state.

Authors:  Jin-Sheng Wu; Ferdinand S Vilim; Nathan G Hatcher; Michael R Due; Jonathan V Sweedler; Klaudiusz R Weiss; Jian Jing
Journal:  J Neurophysiol       Date:  2010-02-24       Impact factor: 2.714

5.  Specificity of repetition priming: the role of chemical coding.

Authors:  Allyson K Friedman; Klaudiusz R Weiss; Elizabeth C Cropper
Journal:  J Neurosci       Date:  2015-04-22       Impact factor: 6.167

6.  Release of a single neurotransmitter from an identified interneuron coherently affects motor output on multiple time scales.

Authors:  Andrew M Dacks; Klaudiusz R Weiss
Journal:  J Neurophysiol       Date:  2013-02-13       Impact factor: 2.714

7.  Repetition priming of motoneuronal activity in a small motor network: intercellular and intracellular signaling.

Authors:  Allyson K Friedman; Klaudiusz R Weiss
Journal:  J Neurosci       Date:  2010-06-30       Impact factor: 6.167

8.  Repetition priming of motor activity mediated by a central pattern generator: the importance of extrinsic vs. intrinsic program initiators.

Authors:  Michael J Siniscalchi; Elizabeth C Cropper; Jian Jing; Klaudiusz R Weiss
Journal:  J Neurophysiol       Date:  2016-07-27       Impact factor: 2.714

9.  Removal of default state-associated inhibition during repetition priming improves response articulation.

Authors:  Andrew M Dacks; Michael J Siniscalchi; Klaudiusz R Weiss
Journal:  J Neurosci       Date:  2012-12-05       Impact factor: 6.167

10.  Complementary interactions between command-like interneurons that function to activate and specify motor programs.

Authors:  Jin-Sheng Wu; Nan Wang; Michael J Siniscalchi; Matthew H Perkins; Yu-Tong Zheng; Wei Yu; Song-an Chen; Ruo-nan Jia; Jia-Wei Gu; Yi-Qing Qian; Yang Ye; Ferdinand S Vilim; Elizabeth C Cropper; Klaudiusz R Weiss; Jian Jing
Journal:  J Neurosci       Date:  2014-05-07       Impact factor: 6.167

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