Literature DB >> 15601944

Different sensory systems share projection neurons but elicit distinct motor patterns.

Dawn M Blitz1, Mark P Beenhakker, Michael P Nusbaum.   

Abstract

Considerable research has focused on issues pertaining to sensorimotor integration, but in most systems precise information remains unavailable regarding the specific pathways by which different sensory systems regulate any single central pattern-generating circuit. We address this issue by determining how two muscle stretch-sensitive neurons, the gastropyloric receptor neurons (GPRs), influence identified projection neurons that regulate the gastric mill circuit in the stomatogastric nervous system of the crab and then comparing these actions with those of the ventral cardiac neuron (VCN) mechanosensory system. Here, we show that the GPR neurons activate the gastric mill rhythm in the stomatogastric ganglion (STG) via their excitation of two identified projection neurons, modulatory commissural neuron 1 (MCN1) and commissural projection neuron 2 (CPN2), in the commissural ganglion. Support for this conclusion comes from the ability of the modulatory proctolin neuron (MPN), a projection neuron that suppresses the gastric mill rhythm via its inhibitory actions on MCN1 and CPN2, to inhibit the GPR-elicited gastric mill rhythm. Selective elimination of MCN1 and CPN2 access to the STG also prevents GPR activation of this rhythm. The VCN neurons also elicit the gastric mill rhythm by coactivating MCN1 and CPN2, but the GPR-elicited gastric mill rhythm is distinct. These distinct rhythms are likely to result partly from different MCN1 activity levels under these two conditions and partly from the presence of additional GPR actions in the STG. These results support the hypothesis that different sensory systems differentially regulate neuronal circuit activity despite their convergent actions on a single subpopulation of projection neurons.

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Year:  2004        PMID: 15601944      PMCID: PMC6494448          DOI: 10.1523/JNEUROSCI.3219-04.2004

Source DB:  PubMed          Journal:  J Neurosci        ISSN: 0270-6474            Impact factor:   6.709


  60 in total

1.  Encoding of muscle movement on two time scales by a sensory neuron that switches between spiking and bursting modes.

Authors:  J T Birmingham; Z B Szuts; L F Abbott; E Marder
Journal:  J Neurophysiol       Date:  1999-11       Impact factor: 2.714

2.  Laser ablations reveal functional relationships of segmental hindbrain neurons in zebrafish.

Authors:  K S Liu; J R Fetcho
Journal:  Neuron       Date:  1999-06       Impact factor: 17.173

3.  Distinct functions for cotransmitters mediating motor pattern selection.

Authors:  D M Blitz; M P Nusbaum
Journal:  J Neurosci       Date:  1999-08-15       Impact factor: 6.167

4.  Coordination of fast and slow rhythmic neuronal circuits.

Authors:  M Bartos; Y Manor; F Nadim; E Marder; M P Nusbaum
Journal:  J Neurosci       Date:  1999-08-01       Impact factor: 6.167

5.  Different proctolin neurons elicit distinct motor patterns from a multifunctional neuronal network.

Authors:  D M Blitz; A E Christie; M J Coleman; B J Norris; E Marder; M P Nusbaum
Journal:  J Neurosci       Date:  1999-07-01       Impact factor: 6.167

6.  A proprioceptive role for an exteroceptive mechanoafferent neuron in Aplysia.

Authors:  D Borovikov; C G Evans; J Jing; S C Rosen; E C Cropper
Journal:  J Neurosci       Date:  2000-03-01       Impact factor: 6.167

7.  Dynamic restructuring of a rhythmic motor program by a single mechanoreceptor neuron in lobster.

Authors:  D Combes; P Meyrand; J Simmers
Journal:  J Neurosci       Date:  1999-05-01       Impact factor: 6.167

8.  Role of proprioceptive signals from an insect femur-tibia joint in patterning motoneuronal activity of an adjacent leg joint.

Authors:  D Hess; A Büschges
Journal:  J Neurophysiol       Date:  1999-04       Impact factor: 2.714

9.  Motor pattern specification by dual descending pathways to a lobster rhythm-generating network.

Authors:  D Combes; P Meyrand; J Simmers
Journal:  J Neurosci       Date:  1999-05-01       Impact factor: 6.167

10.  Diverse synaptic connections between peptidergic radula mechanoafferent neurons and neurons in the feeding system of Aplysia.

Authors:  S C Rosen; M W Miller; C G Evans; E C Cropper; I Kupfermann
Journal:  J Neurophysiol       Date:  2000-03       Impact factor: 2.714

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  38 in total

1.  Peptide neuromodulation of synaptic dynamics in an oscillatory network.

Authors:  Shunbing Zhao; Amir Farzad Sheibanie; Myongkeun Oh; Pascale Rabbah; Farzan Nadim
Journal:  J Neurosci       Date:  2011-09-28       Impact factor: 6.167

2.  Incorporating spike-rate adaptation into a rate code in mathematical and biological neurons.

Authors:  Bridget N Ralston; Lucas Q Flagg; Eric Faggin; John T Birmingham
Journal:  J Neurophysiol       Date:  2016-02-17       Impact factor: 2.714

Review 3.  Animal-to-Animal Variability in Neuromodulation and Circuit Function.

Authors:  Albert W Hamood; Eve Marder
Journal:  Cold Spring Harb Symp Quant Biol       Date:  2015-04-15

4.  A modeling comparison of projection neuron- and neuromodulator-elicited oscillations in a central pattern generating network.

Authors:  Nickolas Kintos; Michael P Nusbaum; Farzan Nadim
Journal:  J Comput Neurosci       Date:  2007-11-29       Impact factor: 1.621

5.  Convergent motor patterns from divergent circuits.

Authors:  Shari R Saideman; Dawn M Blitz; Michael P Nusbaum
Journal:  J Neurosci       Date:  2007-06-20       Impact factor: 6.167

6.  A newly identified extrinsic input triggers a distinct gastric mill rhythm via activation of modulatory projection neurons.

Authors:  Dawn M Blitz; Rachel S White; Shari R Saideman; Aaron Cook; Andrew E Christie; Farzan Nadim; Michael P Nusbaum
Journal:  J Exp Biol       Date:  2008-03       Impact factor: 3.312

7.  Consequences of acute and long-term removal of neuromodulatory input on the episodic gastric rhythm of the crab Cancer borealis.

Authors:  Albert W Hamood; Eve Marder
Journal:  J Neurophysiol       Date:  2015-07-08       Impact factor: 2.714

8.  Multiple mechanisms for integrating proprioceptive inputs that converge on the same motor pattern-generating network.

Authors:  Gregory Barrière; John Simmers; Denis Combes
Journal:  J Neurosci       Date:  2008-08-27       Impact factor: 6.167

Review 9.  Modulation of stomatogastric rhythms.

Authors:  Wolfgang Stein
Journal:  J Comp Physiol A Neuroethol Sens Neural Behav Physiol       Date:  2009-10-11       Impact factor: 1.836

10.  Selective Gating of Neuronal Activity by Intrinsic Properties in Distinct Motor Rhythms.

Authors:  Wen-Chang Li
Journal:  J Neurosci       Date:  2015-07-08       Impact factor: 6.167

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