Hindbrain V2a Neurons in the Excitation of Spinal Locomotor Circuits during Zebrafish Swimming

Kimura, Yukiko; Satou, Chie; Fujioka, Shunji; Watanabe, Shôji; Umeda, Keiko; Ishizuka, Toru; Yawo, Hiromu; Higashijima, Shin‐ichi

doi:10.1016/j.cub.2013.03.066

Cited by 173 publications

(220 citation statements)

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“…For example, reticular neurons in rhombomeres (r) 1-4 in larval zebrafish, including large, ipsilaterally projecting reticulospinal neurons in r4 that are likely to be homologous to pRS neurons in the most caudal portion of the mammalian PRF, have been shown to be involved in regulating the spinal locomotor network (Kimura et al 2013). Startle responses in the zebrafish, however, are abolished by eliminating collectively the contralaterally projecting Mauthner neuron in r4 and its contralaterally projecting medullary segmental homologs, the MiD2cm and MiD3cm neurons in r5 and r6 (Liu and Fetcho 1999).…”

Section: General Overview Of Salient Resultsmentioning

confidence: 99%

Organization of pontine reticulospinal inputs to motoneurons controlling axial and limb muscles in the neonatal mouse

Sivertsen

Glover

Perreault

2014

Journal of Neurophysiology

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Sivertsen MS, Glover JC, Perreault MC. Organization of pontine reticulospinal inputs to motoneurons controlling axial and limb muscles in the neonatal mouse. J Neurophysiol 112: 1628 -1643, 2014. First published June 18, 2014 doi:10.1152/jn.00820.2013.-Using optical recording of synaptically mediated calcium transients and selective spinal lesions, we investigated the pattern of activation of spinal motoneurons (MNs) by the pontine reticulospinal projection in isolated brain stem-spinal cord preparations from the neonatal mouse. Stimulation sites throughout the region where the pontine reticulospinal neurons reside reliably activated MNs at cervical, thoracic, and lumbar levels. Activation was similar in MNs ipsi-and contralateral to the stimulation site, similar in medial and lateral motor columns that contain trunk and limb MNs, respectively, and similar in the L2 and L5 segments that predominantly contain flexor and extensor MNs, respectively. In nonlesioned preparations, responses in both ipsi-and contralateral MNs followed individual stimuli in stimulus trains nearly one-to-one (with few failures). After unilateral hemisection at C1 on the same side as the stimulation, responses had substantially smaller magnitudes and longer latencies and no longer followed individual stimuli. After unilateral hemisection at C1 on the side opposite to the stimulation, the responses were also smaller, but their latencies were not affected. Thus we distinguish two pontine reticulospinal pathways to spinal MNs, one uncrossed and the other crossed, of which the uncrossed pathway transmits more faithfully and appears to be more direct. motor control; descending pathways; brain stem; spinal cord; trunk; limb THE MAMMALIAN RETICULOSPINAL system, consisting of the mesencephalic, pontine, and medullary reticulospinal pathways, is crucial for the control of skeletal musculature (Baker 2011;Kuypers 1964;Lemon 2008;Perreault and Glover 2013;Peterson 1979;Pettersson et al. 2007), but the neural mechanisms by which it initiates and regulates movement are far from understood.Electrical stimulation has been a key method in studying the organization of the mammalian reticulospinal system, revealing excitatory reticulospinal connections (mono-and polysynaptic) with axial motoneurons (MNs), proximal and distal limb MNs, and digit MNs in a variety of species (monkey: Davidson and Buford 2006;Riddle et al. 2009; cat: Drew and Rossignol 1990b;Galea et al. 2010;Grillner et al. 1968;Jankowska et al. 2003;Lloyd 1941;Peterson et al. 1979;Sprague and Chambers 1954;Wilson and Yoshida 1969; rat: Bolzoni et al. 2013; Floeter and Lev-Tov 1993;Umeda et al. 2010; and mouse: Alstermark and Ogawa 2004;Szokol et al. 2008). However, many studies have not differentiated among different areas of the reticular formation (RF) that project to the spinal cord. For example, stimulation of the medial longitudinal fasciculus (MLF), in which many (but certainly not all) reticulospinal axons project, is often used as a proxy for stimulating reticulospinal projectio...

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Section: General Overview Of Salient Resultsmentioning

confidence: 99%

Organization of pontine reticulospinal inputs to motoneurons controlling axial and limb muscles in the neonatal mouse

Sivertsen

Glover

Perreault

2014

Journal of Neurophysiology

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“…Furthermore, our results indicate that this function is primarily carried out by the MeS neuron population, with contributions from MeL cells. This function is likely to be carried out in concert with separate descending motor commands for rhythmic tail oscillations during swimming (Arrenberg et al, 2009; Kimura et al, 2013). …”

Section: Discussionmentioning

confidence: 99%

“…Under this scheme, dedicated modules – as opposed to distributed neural circuits – are responsible for commanding discrete groups of muscles (Briggman and Kristan, 2008). In the context of zebrafish behavior, specific motor components appear to be driven by distinct clusters of neurons, including the speed of the escape-associated C-bend (Liu and Fetcho, 1999; O’Malley et al, 1996; Prugh et al, 1982), spontaneous and stimulus-evoked turning (Huang et al, 2013; Orger et al, 2008), forward swimming (Arrenberg et al, 2009; Kimura et al, 2013) and ballistic eye movements (Schoonheim et al, 2010). We have shown here that activity in a small population of anatomically defined midbrain neurons is necessary and sufficient for controlling swim orientation as part of the optomotor response.…”

Section: Discussionmentioning

confidence: 99%

Descending Control of Swim Posture by a Midbrain Nucleus in Zebrafish

Thiele

Donovan

Baier

2014

Neuron

170

143

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The reticular formation in the brainstem controls motor output via axonal projections to the hindbrain and spinal cord. It remains unclear how individual groups of brainstem neurons contribute to specific motor functions. Here, we investigate the behavioral role of the nucleus of the medial longitudinal fasciculus (nMLF), a small group of reticulospinal neurons in the zebrafish midbrain. Calcium imaging revealed that nMLF activity is correlated with bouts of swimming. Optogenetic stimulation of neurons in the left or right nMLF activates the posterior hypaxial muscle and produces a graded ipsilateral tail deflection. Unilateral ablation of a subset of nMLF cells biases the tail position to the intact side during visually evoked swims, while sparing other locomotor maneuvers. We conclude that activity in the nMLF provides postural control of tail orientation and thus steers the direction of swimming. Our studies provide an example of fine-grained modularity of descending motor control in vertebrates.

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“…The GFP and lRl-GFP (loxP-DsRedloxP-GFP) constructs for homologous recombination were described previously (Kimura et al, 2006). The Gal4 (Gal4FF) (Asakawa et al, 2008) and Cre constructs were described by Kimura et al (Kimura et al, 2013) and Satou et al (Satou et al, 2012), respectively. The lRl-Gal4 construct was prepared by replacing GFP with Gal4 in the lRl-GFP.…”

Section: Generation Of Transgenic Fishmentioning

confidence: 99%

Transgenic tools to characterize neuronal properties of discrete populations of zebrafish neurons

et al. 2013

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SUMMARYThe developing nervous system consists of a variety of cell types. Transgenic animals expressing reporter genes in specific classes of neuronal cells are powerful tools for the study of neuronal network formation. We generated a wide variety of transgenic zebrafish that expressed reporter genes in specific classes of neurons or neuronal progenitors. These include lines in which neurons of specific neurotransmitter phenotypes expressed fluorescent proteins or Gal4, and lines in which specific subsets of the dorsal progenitor domain in the spinal cord expressed fluorescent proteins. Using these, we examined domain organization in the developing dorsal spinal cord, and found that there are six progenitor domains in zebrafish, which is similar to the domain organization in mice. We also systematically characterized neurotransmitter properties of the neurons that are produced from each domain. Given that reporter gene expressions occurs in a wide area of the nervous system in the lines generated, these transgenic fish should serve as powerful tools for the investigation of not only the neurons in the dorsal spinal cord but also neuronal structures and functions in many other regions of the nervous system.

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Hindbrain V2a Neurons in the Excitation of Spinal Locomotor Circuits during Zebrafish Swimming

Abstract: These results indicated that hindbrain reticulospinal V2a neurons play critical roles in providing excitation to the spinal locomotor circuits during swimming by providing both tonic and phasic inputs to the circuits.

Cited by 173 publications

References 38 publications

Organization of pontine reticulospinal inputs to motoneurons controlling axial and limb muscles in the neonatal mouse

Organization of pontine reticulospinal inputs to motoneurons controlling axial and limb muscles in the neonatal mouse

Descending Control of Swim Posture by a Midbrain Nucleus in Zebrafish

Transgenic tools to characterize neuronal properties of discrete populations of zebrafish neurons

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