Spatiotemporal Dynamics of Rhythmic Spinal Interneurons Measured With Two-Photon Calcium Imaging and Coherence Analysis

Kwan, Alex C.; Dietz, Shelby B.; Zhong, Guisheng; Harris-Warrick, Ronald M.; Webb, Watt W.

doi:10.1152/jn.00679.2010

Cited by 28 publications

(27 citation statements)

References 55 publications

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“…In the mouse spinal cord, the rhythmically activeV2a interneurons appear to be recruited more like motoneurons: virtually all increase their activity monotonically with cycle frequency. We have not observed any significant relation between the neuronal location and V2a firing properties during fictive locomotion; Kwan et al (2010) used calcium imaging techniques to monitor V2a activity during fictive locomotion, and did not find any spatial clustering of rhythmically active vs. tonic V2a interneurons 44 . Some V2a neurons start firing at lower frequencies, and increase their activity (action potentials per cycle) as the locomotor speed accelerates (Figs.3 and 6).…”

Section: Discussioncontrasting

confidence: 61%

Frequency-dependent recruitment of V2a interneurons during fictive locomotion in the mouse spinal cord

2011

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The principles governing the recruitment of interneurons during acceleration in vertebrate locomotion are not known. In the mouse, the V2a spinal interneurons are dispensable for left-right coordination at low locomotor frequencies, but their function is essential for maintaining left-right coordination at high frequencies. Here we explore the mechanisms driving this frequency-dependent role, using four methods to determine how V2a interneurons are recruited at different locomotor frequencies. We show that half the V2a interneurons receive rhythmic locomotor synaptic drive which increases with cycle frequency, recruiting more of the neurons to fire at higher frequencies. The other V2a interneurons do not receive locomotion-related synaptic drive, and are not recruited into the locomotor network at any frequency. The increased role of V2a interneurons at higher locomotor frequencies arises from increased synaptic drive to recruit subthreshold oscillating V2a neurons, and not from recruitment of a second set of silent V2a interneurons.

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Section: Discussioncontrasting

confidence: 61%

Frequency-dependent recruitment of V2a interneurons during fictive locomotion in the mouse spinal cord

2011

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“…Second, in contrast to local dye application methods used by others [31], [32], all networks from T13 to L5 were uniformly labeled by bath-application of the membrane permeant indicator. Thus, the observation of locomotor-related activity concentrated at L1 likely indicates functional specialization of networks in this region.…”

Section: Discussionmentioning

confidence: 99%

Functional Organization of Locomotor Interneurons in the Ventral Lumbar Spinal Cord of the Newborn Rat

2011

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Although the mammalian locomotor CPG has been localized to the lumbar spinal cord, the functional-anatomical organization of flexor and extensor interneurons has not been characterized. Here, we tested the hypothesis that flexor and extensor interneuronal networks for walking are physically segregated in the lumbar spinal cord. For this purpose, we performed optical recordings and lesion experiments from a horizontally sectioned lumbar spinal cord isolated from neonate rats. This ventral hemi spinal cord preparation produces well-organized fictive locomotion when superfused with 5-HT/NMDA. The dorsal surface of the preparation was visualized using the Ca2+ indicator fluo-4 AM, while simultaneously monitoring motor output at ventral roots L2 and L5. Using calcium imaging, we provided a general mapping view of the interneurons that maintained a stable phase relationship with motor output. We showed that the dorsal surface of L1 segment contains a higher density of locomotor rhythmic cells than the other segments. Moreover, L1 segment lesioning induced the most important changes in the locomotor activity in comparison with lesions at the T13 or L2 segments. However, no lesions led to selective disruption of either flexor or extensor output. In addition, this study found no evidence of functional parcellation of locomotor interneurons into flexor and extensor pools at the dorsal-ventral midline of the lumbar spinal cord of the rat.

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“…5, 6), we find that although mixed, flexor interneurons predominate rostrally, and extensor interneurons caudally. This relates to in vitro locomotion results of a mixture of preferred interneuronal firing phases in each segment, but more often in phase with the segment output, flexor in L2, and extensor in L5 (Tresch and Kiehn 1999;Cheng et al 2002;Kwan et al 2010;Dougherty and Kiehn 2010;Zhong et al 2010, but see Auyong et al 2011;Antri et al 2011;Hinckley and Pfaff 2013, who found no correlation between firing phase and rostrocaudal location). The overlap of the preferred zones of activation of different synergies in Figs.…”

Section: Topography Of Synergiesmentioning

confidence: 99%

Synergy temporal sequences and topography in the spinal cord: evidence for a traveling wave in frog locomotion

et al. 2015

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Locomotion is produced by a central pattern generator. Its spinal cord organization is generally considered to be distributed, with more rhythmogenic rostral lumbar segments. While this produces a rostrocaudally traveling wave in undulating species, this is not thought to occur in limbed vertebrates, with the exception of the interneuronal traveling wave demonstrated in fictive cat scratching (Cuellar et al. J Neurosci 29:798-810, 2009). Here, we reexamine this hypothesis in the frog, using the seven muscle synergies A to G previously identified with intraspinal NMDA (Saltiel et al. J Neurophysiol 85:605-619, 2001). We find that locomotion consists of a sequence of synergy activations (A-B-G-A-F-E-G). The same sequence is observed when focal NMDA iontophoresis in the spinal cord elicits a caudal extensionlateral force-flexion cycle (flexion onset without the C synergy). Examining the early NMDA-evoked motor output at 110 sites reveals a rostrocaudal topographic organization of synergy encoding by the lumbar cord. Each synergy is preferentially activated from distinct regions, which may be multiple, and partially overlap between different synergies. Comparing the sequence of synergy activation in locomotion with their spinal cord topography suggests that the locomotor output is achieved by a rostrocaudally traveling wave of activation in the swing-stance cycle. A two-layer circuitry model, based on this topography and a traveling wave reproduces this output and explores its possible modifications under different afferent inputs. Our results and simulations suggest that a rostrocaudally traveling wave of excitation takes advantage of the topography of interneuronal regions encoding synergies, to activate them in the proper sequence for locomotion.

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Spatiotemporal Dynamics of Rhythmic Spinal Interneurons Measured With Two-Photon Calcium Imaging and Coherence Analysis

Cited by 28 publications

References 55 publications

Frequency-dependent recruitment of V2a interneurons during fictive locomotion in the mouse spinal cord

Frequency-dependent recruitment of V2a interneurons during fictive locomotion in the mouse spinal cord

Functional Organization of Locomotor Interneurons in the Ventral Lumbar Spinal Cord of the Newborn Rat

Synergy temporal sequences and topography in the spinal cord: evidence for a traveling wave in frog locomotion

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