Gap Junction–Mediated Signaling from Motor Neurons Regulates Motor Generation in the Central Circuits of Larval<i>Drosophila</i>

Matsunaga, Teruyuki; Kohsaka, Hiroshi; Nose, Akinao

doi:10.1523/jneurosci.1453-16.2017

Cited by 28 publications

(28 citation statements)

References 56 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…As described above, this would lead to a change in the firing frequency of VPN neurons and thus modify VMN activity. Similar motor–premotor coupling has recently been shown in zebrafish and Drosophila locomotor networks in regard to motor rhythm control (Matsunaga, Kohsaka, & Nose, ), as well as in the Xenopus vocal pattern generator (Lawton, Perry, Yamaguchi, & Zornik, ).…”

Section: Discussionsupporting

confidence: 65%

“…Electrophysiological recordings from VPN in midshipman fish strengthen this hypothesis as current injection into VPN neurons does not induce the characteristic firing frequency displayed during vocal activity (Chagnaud et al, 2012). (Matsunaga, Kohsaka, & Nose, 2017), as well as in the Xenopus vocal pattern generator (Lawton, Perry, Yamaguchi, & Zornik, 2017).…”

Section: Gabamentioning

confidence: 88%

See 1 more Smart Citation

Inhibitory and modulatory inputs to the vocal central pattern generator of a teleost fish

Rosner

Rohmann

Bass

et al. 2018

J of Comparative Neurology

View full text Add to dashboard Cite

Vocalization is a behavioral feature that is shared among multiple vertebrate lineages, including fish. The temporal patterning of vocal communication signals is set, in part, by central pattern generators (CPGs). Toadfishes are well‐established models for CPG coding of vocalization at the hindbrain level. The vocal CPG comprises three topographically separate nuclei: pre‐pacemaker, pacemaker, motor. While the connectivity between these nuclei is well understood, their neurochemical profile remains largely unexplored. The highly vocal Gulf toadfish, Opsanus beta, has been the subject of previous behavioral, neuroanatomical and neurophysiological studies. Combining transneuronal neurobiotin‐labeling with immunohistochemistry, we map the distribution of inhibitory neurotransmitters and neuromodulators along with gap junctions in the vocal CPG of this species. Dense GABAergic and glycinergic label is found throughout the CPG, with labeled somata immediately adjacent to or within CPG nuclei, including a distinct subset of pacemaker neurons co‐labeled with neurobiotin and glycine. Neurobiotin‐labeled motor and pacemaker neurons are densely co‐labeled with the gap junction protein connexin 35/36, supporting the hypothesis that transneuronal neurobiotin‐labeling occurs, at least in part, via gap junction coupling. Serotonergic and catecholaminergic label is also robust within the entire vocal CPG, with additional cholinergic label in pacemaker and prepacemaker nuclei. Likely sources of these putative modulatory inputs are neurons within or immediately adjacent to vocal CPG neurons. Together with prior neurophysiological investigations, the results reveal potential mechanisms for generating multiple classes of social context‐dependent vocalizations with widely divergent temporal and spectral properties.

show abstract

Section: Discussionsupporting

confidence: 65%

Section: Gabamentioning

confidence: 88%

Inhibitory and modulatory inputs to the vocal central pattern generator of a teleost fish

Rosner

Rohmann

Bass

et al. 2018

J of Comparative Neurology

View full text Add to dashboard Cite

show abstract

“…The intrinsic activity of the AS MNs correlates best with forward locomotion, which corresponds to a stronger response of AS MNs to photodepolarization of the forward PIN AVB. Functionally asymmetric electrical connections suggest AS MN feedback control of the backward PIN AVA, a feature recently observed for locomotor circuits also in other animals (Matsunaga et al, 2017; Song et al, 2016).…”

Section: Introductionsupporting

confidence: 59%

“…Despite anatomical prevalence of chemical synapses from AVA to AS MNs, our data showed larger AS MN effects after stimulation of the forward PIN AVB, and a stronger correlation of AS MN activity with forward locomotion. Recently, ability of MNs to modulate activity of PINs was shown in several animal models: for B-type MNs changing the inhibitory chemical transmission of AVB to AVA in C. elegans (Kawano et al, 2011; Liu et al, 2017); for MNs regulating the frequency of crawling in Drosophila (Matsunaga et al, 2017); for MNs affecting activity of the excitatory V2a neurons in zebrafish (Song et al, 2016); and, in the mouse, such activity was suggested for MNs, changing the frequency of rhythmic CPG activity after stimulation by rhodopsins (Falgairolle et al, 2017). Positive feedback from MNs required the function of gap junctions, coupling between MNs and PINs in all these systems.…”

Section: Discussionmentioning

confidence: 99%

Functionally asymmetric motor neurons coordinate locomotion of Caenorhabditis elegans

Tolstenkov

Auwera

Liewald

et al. 2018

Preprint

View full text Add to dashboard Cite

show abstract

“…This points to the possibility of a dedicated D1-dependent circuit that could underlie the generation of rhythmic activities elicited by high concentrations of dopamine. Motoneurons compose key rhythm generating elements in invertebrate circuits [66][67][68] and also participate in rhythm generation in vertebrates [69], including rodents [32,40,56,70,71]. V3 interneurons are one subclass of geneticallydefined spinal interneuron that are important for the generation of rhythmic activities in mammalian spinal networks [53,55,72] and receive recurrent excitatory collaterals from motoneurons in rodents [32].…”

Section: Dedicated Network Components Segregate Excitatory and Inhibimentioning

confidence: 99%

A dynamic role for dopamine receptors in the control of mammalian spinal networks

Sharples

Burma

Borowska-Fielding

et al. 2019

Preprint

View full text Add to dashboard Cite

Dopamine is well known to regulate movement through the differential control of direct and indirect pathways in the striatum that express D1 and D2 receptors respectively. The spinal cord also expresses all dopamine receptors however; how the specific receptors regulate spinal network output in mammals is poorly understood. We explore the receptor-specific mechanisms that underlie dopaminergic control of spinal network output of neonatal mice during changes in spinal network excitability. During spontaneous activity, which is a characteristic of developing spinal networks operating in a low excitability state, we found that dopamine is primarily inhibitory. We uncover an excitatory D1-mediated effect of dopamine on motoneurons and network output that also involves co-activation with D2 receptors. Critically, these excitatory actions require higher concentrations of dopamine; however, analysis of dopamine concentrations of neonates indicates that endogenous levels of spinal dopamine are low. Because endogenous levels of spinal dopamine are low, this excitatory dopaminergic pathway is likely physiologically-silent at this stage in development. In contrast, the inhibitory effect of dopamine, at low physiological concentrations is mediated by parallel activation of D2, D3, D4 and α2 receptors which is reproduced when endogenous dopamine levels are increased by blocking dopamine reuptake and metabolism. We provide evidence in support of dedicated spinal network components that are controlled by excitatory D1 and inhibitory D2 receptors that is reminiscent of the classic dopaminergic indirect and direct pathway within the striatum. These results indicate that network state is an important factor that dictates receptor-specific and therefore dose-dependent control of neuromodulators on spinal network output and advances our understanding of how neuromodulators regulate neural networks under dynamically changing excitability.Significance statement: Monoaminergic neuromodulation of neural networks is dependent not only on target receptors but also on network state. We studied the concentration-dependent control of spinal networks of the neonatal mouse, in vitro, during a low excitability state characterized by spontaneous network activity. Spontaneous activity is an essential element for the development of networks. Under these conditions, we defined converging receptor and cellular mechanisms that contribute to the diverse, concentration-dependent control of spinal motor networks by dopamine, in vitro. These experiments advance understanding of how monoamines modulate neuronal networks under dynamically changing excitability conditions and provide evidence of dedicated D1 and D2 regulated network components in the spinal cord that are consistent with those reported in the striatum.

show abstract

Gap Junction–Mediated Signaling from Motor Neurons Regulates Motor Generation in the Central Circuits of LarvalDrosophila

Cited by 28 publications

References 56 publications

Inhibitory and modulatory inputs to the vocal central pattern generator of a teleost fish

Inhibitory and modulatory inputs to the vocal central pattern generator of a teleost fish

Functionally asymmetric motor neurons coordinate locomotion of Caenorhabditis elegans

A dynamic role for dopamine receptors in the control of mammalian spinal networks

Contact Info

Product

Resources

About