From lamprey to salamander: an exploratory modeling study on the architecture of the spinal locomotor networks in the salamander

Bičanski, Andrej; Ryczko, Dimitri; Cabelguen, Jean-Marie; Ijspeert, Auke Jan

doi:10.1007/s00422-012-0538-y

Cited by 28 publications

(30 citation statements)

References 148 publications

(240 reference statements)

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“…These other treatment conditions may include modulation or removal of subsets of currents that elicit characteristic oscillatory behaviors such as seizure-like activities or slow subthreshold oscillations (Grillner et al, 1995; Cymbalyuk and Calabrese, 2000, 2001; Krishnan and Bazhenov, 2011; Jasinski et al, 2013; Barnett et al, 2013; Bicanski et al, 2013; Doloc-Mihu and Calabrese, 2014; Krishnan et al, 2015). Moreover, the greater sensitivity of the model without h -current to the monensin rate constant suggests that the h -current plays a protective role to prevent disruption of functional activity in oscillator heart interneurons, consistent with previous observations (Cymbalyuk et al, 2002; Marin et al, 2013).…”

Section: Discussionmentioning

confidence: 99%

Na+/K+ pump interacts with the h-current to control bursting activity in central pattern generator neurons of leeches

Kueh

Barnett

Cymbalyuk

et al. 2016

eLife

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The dynamics of different ionic currents shape the bursting activity of neurons and networks that control motor output. Despite being ubiquitous in all animal cells, the contribution of the Na+/K+ pump current to such bursting activity has not been well studied. We used monensin, a Na+/H+ antiporter, to examine the role of the pump on the bursting activity of oscillator heart interneurons in leeches. When we stimulated the pump with monensin, the period of these neurons decreased significantly, an effect that was prevented or reversed when the h-current was blocked by Cs+. The decreased period could also occur if the pump was inhibited with strophanthidin or K+-free saline. Our monensin results were reproduced in model, which explains the pump’s contributions to bursting activity based on Na+ dynamics. Our results indicate that a dynamically oscillating pump current that interacts with the h-current can regulate the bursting activity of neurons and networks.DOI: http://dx.doi.org/10.7554/eLife.19322.001

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Section: Discussionmentioning

confidence: 99%

Na+/K+ pump interacts with the h-current to control bursting activity in central pattern generator neurons of leeches

Kueh

Barnett

Cymbalyuk

et al. 2016

eLife

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“…The anatomy of the RS system was described in this animal by tracing studies (Naujoks‐Manteuffel and Manteuffel, ; Sanchez‐Camacho et al, ; Hubbard et al, ) and some RS cells were shown to be glutamatergic (Chevallier et al, ). The key role of RS cells in controlling the spinal locomotor CPG was recently modeled (Bicanski et al, ). The salamander MLR controls locomotor output (Cabelguen et al, ), and we now show that the strength of MLR stimulation controls the Ca 2+ responses of RS neurons of the rostral and caudal hindbrain.…”

Section: Discussionmentioning

confidence: 99%

The mesencephalic locomotor region sends a bilateral glutamatergic drive to hindbrain reticulospinal neurons in a tetrapod

Ryczko

Auclair

Cabelguen

et al. 2015

J of Comparative Neurology

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105

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In vertebrates, stimulation of the mesencephalic locomotor region (MLR) on one side evokes symmetrical locomotor movements on both sides. How this occurs was previously examined in detail in a swimmer using body undulations (lamprey), but in tetrapods the downstream projections from the MLR to brainstem neurons are not fully understood. Here we examined the brainstem circuits from the MLR to identified reticulospinal neurons in the salamander Notophthalmus viridescens. Using neural tracing, we show that the MLR sends bilateral projections to the middle reticular nucleus (mRN, rostral hindbrain) and the inferior reticular nucleus (iRN, caudal hindbrain). Ca2+ imaging coupled to electrophysiology in in vitro isolated brains revealed very similar responses in reticulospinal neurons on both sides to a unilateral MLR stimulation. As the strength of MLR stimulation was increased, the responses increased in size in reticulospinal neurons of the mRN and iRN, but the responses in the iRN were smaller. Bath‐application or local microinjections of glutamatergic antagonists markedly reduced reticulospinal neuron responses, indicating that the MLR sends glutamatergic inputs to reticulospinal neurons. In addition, reticulospinal cells responded to glutamate microinjections and the size of the responses paralleled the amount of glutamate microinjected. Immunofluorescence coupled with anatomical tracing confirmed the presence of glutamatergic projections from the MLR to reticulospinal neurons. Overall, we show that the brainstem circuits activated by the MLR in the salamander are organized similarly to those previously described in lampreys, indicating that the anatomo‐physiological features of the locomotor drive are well conserved in vertebrates. J. Comp. Neurol. 524:1361–1383, 2016. © 2015 The Authors The Journal of Comparative Neurology Published by Wiley Periodicals, Inc.

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“…Based on these new findings, we have recently proposed a tentative model of axial spinal segments and hemisegments of the salamander spinal cord at the cellular level, using a biophysical model adapted from the lamprey literature (Bicanski et al 2011(Bicanski et al , 2012, in the same issue). The neuron model was a simplified version of the multicompartment Hodgkin-Huxley model used by Wallén et al (1992) (reduced from 5 to 3 compartments).…”

Section: The Trunk Networkmentioning

confidence: 99%

“…Both E and C populations have axons extending longer in the caudal direction. C Segmental network in Bicanski et al (2012).…”

Section: The Tail Networkmentioning

confidence: 99%

Decoding the mechanisms of gait generation in salamanders by combining neurobiology, modeling and robotics

et al. 2013

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Vertebrate animals exhibit impressive locomotor skills. These locomotor skills are due to the complex interactions between the environment, the musculo-skeletal system and the central nervous system, in particular the spinal locomotor circuits. We are interested in decoding these interactions in the salamander, a key animal from an evolutionary point of view. It exhibits both swimming and stepping gaits and is faced with the problem of producing efficient propulsive forces using the same musculo-skeletal system in two environments with significant physical differences in density, viscosity and gravitational load. Yet its nervous system remains comparatively simple. Our approach is based on a combination of neurophysiological experiments, numerical modeling at different levels of abstraction, and robotic validation using an amphibious salamander-like robot. This article reviews the current state of our knowledge on salamander locomotion control, and presents how our approach has allowed us to obtain a first conceptual model of the salamander spinal locomotor networks. The model suggests that the salamander locomotor circuit can be seen as a lamprey-like circuit controlling axial movements of the trunk and tail, extended by specialized oscillatory centers controlling limb movements. The interplay between the two types of circuits determines the mode of locomotion under the influence of sensory feedback and descending drive, with stepping gaits at low drive, and swimming at high drive.

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From lamprey to salamander: an exploratory modeling study on the architecture of the spinal locomotor networks in the salamander

Cited by 28 publications

References 148 publications

Na+/K+ pump interacts with the h-current to control bursting activity in central pattern generator neurons of leeches

Na+/K+ pump interacts with the h-current to control bursting activity in central pattern generator neurons of leeches

The mesencephalic locomotor region sends a bilateral glutamatergic drive to hindbrain reticulospinal neurons in a tetrapod

Decoding the mechanisms of gait generation in salamanders by combining neurobiology, modeling and robotics

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