Sub-populations of Spinal V3 Interneurons Form Focal Modules of Layered Pre-motor Microcircuits

Chopek, Jeremy W.; Nascimento, Filipe; Beato, Marco; Brownstone, Robert M.; Zhang, Ying

doi:10.1016/j.celrep.2018.08.095

Cited by 82 publications

(86 citation statements)

References 64 publications

(105 reference statements)

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“…V3 interneurons represent an additional class of commissural excitatory interneurons that are broadly distributed along the dorsal-ventral and rostral-caudal axes in the postnatal spinal cord (50,52,487). It has been shown that V3 interneurons, in addition to their commissural role, also provide ipsilateral excitation to each other and to motoneurons on the same side (96). Acute silencing of interneurons in the lumbar region of freely moving adult mice produced uneven gaits, suggesting that they play a role in limb coordination (487).…”

Section: ) (Figure 14c)mentioning

confidence: 99%

Current Principles of Motor Control, with Special Reference to Vertebrate Locomotion

Grillner

Manira

2020

Physiological Reviews

361

395

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The vertebrate control of locomotion involves all levels of the nervous system from cortex to the spinal cord. Here, we aim to cover all main aspects of this complex behavior, from the operation of the microcircuits in the spinal cord to the systems and behavioral levels and extend from mammalian locomotion to the basic undulatory movements of lamprey and fish. The cellular basis of propulsion represents the core of the control system, and it involves the spinal central pattern generator networks (CPGs) controlling the timing of different muscles, the sensory compensation for perturbations, and the brain stem command systems controlling the level of activity of the CPGs and the speed of locomotion. The forebrain and in particular the basal ganglia are involved in determining which motor programs should be recruited at a given point of time and can both initiate and stop locomotor activity. The propulsive control system needs to be integrated with the postural control system to maintain body orientation. Moreover, the locomotor movements need to be steered so that the subject approaches the goal of the locomotor episode, or avoids colliding with elements in the environment or simply escapes at high speed. These different aspects will all be covered in the review.

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Section: ) (Figure 14c)mentioning

confidence: 99%

Current Principles of Motor Control, with Special Reference to Vertebrate Locomotion

Grillner

Manira

2020

Physiological Reviews

361

395

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“…A more recent set of experiments described excitatory motor neuron connectivity to one class of non-Renshaw interneuron. Chopek et al (2018) found that motor neurons in postnatal mice activate a population of ipsilateral V3 interneurons via glutamatergic synapses; V3 interneurons, in turn, project bilaterally to neurons in the locomotor CPG. When V3 interneuron signaling is suppressed, locomotor patterns become more variable and left-right alternation is disrupted, suggesting that V3 interneurons maintain robust, bilaterally symmetric locomotor rhythms (Zhang et al, 2008).…”

Section: Chordatamentioning

confidence: 99%

Feedback to the future: motor neuron contributions to central pattern generator function

Barkan

Zornik

2019

Journal of Experimental Biology

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Motor behaviors depend on neural signals in the brain. Regardless of where in the brain behavior patterns arise, the central nervous system sends projections to motor neurons, which in turn project to and control temporally appropriate muscle contractions; thus, motor neurons are traditionally considered the last relay from the central nervous system to muscles. However, in an array of species and motor systems, an accumulating body of evidence supports a more complex role of motor neurons in pattern generation. These studies suggest that motor neurons not only relay motor patterns to the periphery, but directly contribute to pattern generation by providing feedback to upstream circuitry. In spinal and hindbrain circuits in a variety of animalsincluding flies, worms, leeches, crustaceans, rodents, birds, fish, amphibians and mammalsstudies have indicated a crucial role for motor neuron feedback in maintaining normal behavior patterns dictated by the activity of a central pattern generator. Hence, in this Review, we discuss literature examining the role of motor neuron feedback across many taxa and behaviors, and set out to determine the prevalence of motor neuron participation in motor circuits.

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“…In the current study, novel optogenetic tools have enabled us to specifically Hägglund et al, 2013;Levine et al, 2014), reversibly, and acutely regulate the activity of a molecularly-identified group of spinal neurons. By using Sim1Cre/+; Ai32 mice (Chopek et al, 2018), we were able to target V3 interneurons on both or just one side of the isolated spinal cords allowing us to start dissecting the function of V3 CINs in spinal locomotor circuits.…”

Section: Optogenetic Activation Of V3 Interneuronsmentioning

confidence: 99%

Spinal V3 interneurons and left-right coordination in mammalian locomotion

Danner

Zhang

Shevtsova

et al. 2019

Preprint

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Commissural interneurons (CINs) mediate interactions between rhythm-generating locomotor circuits located on each side of the spinal cord and are necessary for left-right limb coordination during locomotion. While glutamatergic V3 CINs have been implicated in left-right coordination, their functional connectivity remains elusive. Here, we addressed this issue by combining experimental and modeling approaches. We employed Sim1Cre/+; Ai32 mice, in which light-activated Channelrhodopsin-2 was selectively expressed in V3 interneurons. Fictive locomotor activity was evoked by NMDA and 5-HT in the isolated neonatal lumbar spinal cord. Flexor and extensor activities were recorded from left and right L2 and L5 ventral roots, respectively. Bilateral photoactivation of V3 interneurons increased the duration of extensor bursts resulting in a slowed down on-going rhythm. At high light intensities, extensor activity could become sustained. When light stimulation was shifted toward one side of the cord, the duration of extensor bursts still increased on both sides, but these changes were more pronounced on the contralateral side than on the ipsilateral side. Additional bursts appeared on the ipsilateral side not seen on the contralateral side. Further increase of the stimulation could suppress the contralateral oscillations by switching to a sustained extensor activity, while the ipsilateral rhythmic activity remained. To delineate the function of V3 interneurons and their connectivity, we developed a computational model of the spinal circuits consisting of two (left and right) rhythm generators (RGs) interacting via V0V, V0D and V3 CINs. Both types of V0 CINs provided mutual inhibition between the left and right flexor RG centers and promoted left-right alternation. V3 CINs mediated mutual excitation between the left and right extensor RG centers. These interactions allowed the model to reproduce our current experimental data, while being consistent with previous data concerning the role of V0V and V0D CINs in securing left-right alternation and the changes in leftright coordination following their selective removal. We suggest that V3 CINs provide mutual excitation between the spinal neurons involved in the control of left and right extensor activity, which may promote left-right synchronization during locomotion. V3 interneurons and left-right coordination2

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Sub-populations of Spinal V3 Interneurons Form Focal Modules of Layered Pre-motor Microcircuits

Cited by 82 publications

References 64 publications

Current Principles of Motor Control, with Special Reference to Vertebrate Locomotion

Current Principles of Motor Control, with Special Reference to Vertebrate Locomotion

Feedback to the future: motor neuron contributions to central pattern generator function

Spinal V3 interneurons and left-right coordination in mammalian locomotion

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