scholarly journals Episodic swimming in the larval zebrafish is generated by a spatially distributed spinal network with modular functional organization

2012 ◽  
Vol 108 (3) ◽  
pp. 925-934 ◽  
Author(s):  
Timothy D. Wiggin ◽  
Tatiana M. Anderson ◽  
John Eian ◽  
Jack H. Peck ◽  
Mark A. Masino

Despite the diverse methods vertebrates use for locomotion, there is evidence that components of the locomotor central pattern generator (CPG) are conserved across species. When zebrafish begin swimming early in development, they perform short episodes of activity separated by periods of inactivity. Within these episodes, the trunk flexes with side-to-side alternation and the traveling body wave progresses rostrocaudally. To characterize the distribution of the swimming CPG along the rostrocaudal axis, we performed transections of the larval zebrafish spinal cord and induced fictive swimming using N-methyl-d-aspartate (NMDA). In both intact and spinalized larvae, bursting is found throughout the rostrocaudal extent of the spinal cord, and the properties of fictive swimming observed were dependent on the concentration of NMDA. We isolated series of contiguous spinal segments by performing multiple spinal transections on the same larvae. Although series from all regions of the spinal cord have the capacity to produce bursts, the capacity to produce organized episodes of fictive swimming has a rostral bias: in the rostral spinal cord, only 12 contiguous body segments are necessary, whereas 23 contiguous body segments are necessary in the caudal spinal cord. Shorter series of segments were often active but produced either continuous rhythmic bursting or sporadic, nonrhythmic bursting. Both episodic and continuous bursting alternated between the left and right sides of the body and showed rostrocaudal progression, demonstrating the functional dissociation of the circuits responsible for episodic structure and fine burst timing. These findings parallel results in mammalian locomotion, and we propose a hierarchical model of the larval zebrafish swimming CPG.

2003 ◽  
Vol 90 (5) ◽  
pp. 3161-3167 ◽  
Author(s):  
P. V. Zelenin ◽  
E. L. Pavlova ◽  
S. Grillner ◽  
G. N. Orlovsky ◽  
T. G. Deliagina

In the lamprey (a lower vertebrate), motor commands from the brain to the spinal cord are transmitted through the reticulospinal (RS) and vestibulospinal (VS) pathways. The axons of larger RS neurons reach the most caudal of approximately 100 spinal segments, whereas the VS pathway does not descend below the 15th segment. This study was carried out to compare functional projections of RS and VS neurons in the rostral spinal segments that the neurons innervate together. To reveal these projections, individual RS or VS neurons were stimulated, and the responses of different groups of spinal motoneurons were recorded in ventral root branches to dorsal and ventral parts of myotomes. The responses were detected using a spike-triggered averaging technique on the background of ongoing motoneuronal activity. Individual RS and VS neurons exerted uniform effects on segmental motor output within this rostral part of the spinal cord. The effects of VS neurons on different groups of motoneurons were weaker and less diverse than those of RS neurons. The results indicate that VS neurons are able to elicit a flexion of the rostral part of the body and to turn the head in different planes without affecting more caudal parts. By contrast, larger RS neurons can elicit head movement only together with movement of a considerable part of the body and thus seem to be responsible for formation of gross motor synergies.


2017 ◽  
Author(s):  
William Olson ◽  
Ishmail Abdus-Saboor ◽  
Lian Cui ◽  
Justin Burdge ◽  
Tobias Raabe ◽  
...  

AbstractThe human distal limbs have a high spatial acuity for noxious stimuli but a low density of pain-sensing neurites. To elucidate mechanisms underlying the ‘pain fovea’, we sparsely traced non-peptidergic nociceptors across the body using a newly generated MrgprDCreERT2 mouse line. We found that mouse plantar paw skin also has a low density of MrgprD+ neurites, and individual arbors in different locations are comparable in size. Surprisingly, the central arbors of plantar paw and trunk innervating nociceptors have distinct morphologies in the spinal cord. This regional difference is well correlated with a heightened signal transmission for plantar paw circuits, as revealed by both spinal cord slice recordings and behavior assays. Taken together, our results elucidate a novel somatotopic functional organization of the mammalian pain system and suggest that regional central arbor structure could facilitate the magnification of plantar paw regions to contribute to the ‘pain fovea’.


eLife ◽  
2017 ◽  
Vol 6 ◽  
Author(s):  
William Olson ◽  
Ishmail Abdus-Saboor ◽  
Lian Cui ◽  
Justin Burdge ◽  
Tobias Raabe ◽  
...  

The human distal limbs have a high spatial acuity for noxious stimuli but a low density of pain-sensing neurites. To elucidate mechanisms underlying regional differences in processing nociception, we sparsely traced non-peptidergic nociceptors across the body using a newly generated MrgprdCreERT2 mouse line. We found that mouse plantar paw skin is also innervated by a low density of Mrgprd+ nociceptors, while individual arbors in different locations are comparable in size. Surprisingly, the central arbors of plantar paw and trunk innervating nociceptors have distinct morphologies in the spinal cord. This regional difference is well correlated with a heightened signal transmission for plantar paw circuits, as revealed by both spinal cord slice recordings and behavior assays. Taken together, our results elucidate a novel somatotopic functional organization of the mammalian pain system and suggest that regional central arbor structure could facilitate the “enlarged representation” of plantar paw regions in the CNS.


eLife ◽  
2019 ◽  
Vol 8 ◽  
Author(s):  
Rebecca A Callahan ◽  
Richard Roberts ◽  
Mohini Sengupta ◽  
Yukiko Kimura ◽  
Shin-ichi Higashijima ◽  
...  

The spinal cord contains a diverse array of interneurons that govern motor output. Traditionally, models of spinal circuits have emphasized the role of inhibition in enforcing reciprocal alternation between left and right sides or flexors and extensors. However, recent work has shown that inhibition also increases coincident with excitation during contraction. Here, using larval zebrafish, we investigate the V2b (Gata3+) class of neurons, which contribute to flexor-extensor alternation but are otherwise poorly understood. Using newly generated transgenic lines we define two stable subclasses with distinct neurotransmitter and morphological properties. These V2b subclasses synapse directly onto motor neurons with differential targeting to speed-specific circuits. In vivo, optogenetic manipulation of V2b activity modulates locomotor frequency: suppressing V2b neurons elicits faster locomotion, whereas activating V2b neurons slows locomotion. We conclude that V2b neurons serve as a brake on axial motor circuits. Together, these results indicate a role for ipsilateral inhibition in speed control.


1993 ◽  
Vol 69 (3) ◽  
pp. 868-883 ◽  
Author(s):  
I. Euchner-Wamser ◽  
J. N. Sengupta ◽  
G. F. Gebhart ◽  
S. T. Meller

1. Three hundred fifty neurons in the T2-T4 spinal segments of 38 intact, pentobarbital sodium-anesthetized, pancuronium-paralyzed male rats were examined for somatic receptive fields and responses to midthoracic esophageal distension (ED). Recordings were made at a depth of 0.1–1.45 mm from the dorsal spinal cord surface and from the midline to approximately 1.0 mm lateral. 2. Fifty-six of the 350 total neurons (16%) responded to ED, produced by air inflation of a latex balloon (0.5–1.5 ml). Most of these 56 neurons (84%) were excited by ED, and all except one were excited at a short latency (< 2 s) to stimulus onset. The response to ED in about one-half of all excited neurons terminated abruptly with termination of the stimulus; the other neurons exhibited an afterdischarge of 5 to > 80 s. Repeated ED at a constant intensity (1.25 ml, 30 s every 6 min) produced stable and reproducible responses of neurons excited by ED. Twenty-one percent of neurons that responded to ED were antidromically invaded from the spinomedullary junction. 3. Graded ED (0.5–1.5 ml, 30 s every 6 min) produced linear and accelerating stimulus-response functions in the 29 neurons tested. The mean threshold for distension, determined with a least-squares regression analysis, was extrapolated to near 0.5 ml of distending volume, and no difference in response threshold was found between neuronal groups with or without after-discharge. 4. The spontaneous activity of 7 of the 56 neurons (12.5%) that responded to ED was inhibited by the stimulus. Stimulus-response functions for four neurons inhibited by ED were intensity dependent. The spontaneous activity of these neurons was inhibited to a mean of 24.5% of the prestimulus control by 1.25 ml ED. 5. Two neurons of the total sample of 56 (3.5%) responded to ED (1.50 ml) in a biphasic excitatory-inhibitory manner. The excitatory component of excitatory-inhibitory neurons encoded the intensity of ED; the inhibitory component during the second half of ED was apparent only at greater distending volumes (1.25–1.5 ml). 6. Somatic receptive fields were found for 303/350 neurons, and 98% were located on the thorax and proximal forearm (all ipsilateral). Five neurons in T2–T4 spinal segments had their cutaneous receptive fields located on caudal parts of the body (tail, hindleg, scrotum).(ABSTRACT TRUNCATED AT 400 WORDS)


Author(s):  
Georgy Bakalkin ◽  
Olga Nosova ◽  
Daniil Sarkisyan ◽  
Mathias Hallberg ◽  
Mengliang Zhang ◽  
...  

AbstractTraumatic brain injury and stroke result in hemiplegia, hemiparesis, and asymmetry in posture. The effects are mostly contralateral; however, ipsilesional deficits may also develop. We here examined whether ablation brain injury and controlled cortical impact (CCI), a rat model of clinical focal traumatic brain injury, both centered over the left or right sensorimotor cortex, induced hindlimb postural asymmetry (HL-PA) with contralesional or ipsilesional limb flexion. The contralesional hindlimb was flexed after left or right side ablation injury. In contrast, both the left and right CCI unexpectedly produced HL-PA with flexion on left side. The flexion persisted after complete spinal cord transection suggesting that CCI triggered neuroplastic processes in lumbar neural circuits enabling asymmetric muscle contraction. Left limb flexion was exhibited under pentobarbital anesthesia. However, under ketamine anesthesia, the body of the left and right CCI rats bent laterally in the coronal plane to the ipsilesional side suggesting that the left and right injury engaged mirror-symmetrical motor pathways. Thus, the effects of the left and right CCI on HL-PA were not mirror-symmetrical in contrast to those of the ablation brain injury, and to the left and right CCI produced body bending. Ipsilateral effects of the left CCI on HL-PA may be mediated by a lateralized motor pathway that is not affected by the left ablation injury. Alternatively, the left-side-specific neurohormonal mechanism that signals from injured brain to spinal cord may be activated by both the left and right CCI but not by ablation injury.


2021 ◽  
Author(s):  
Marco Capogrosso ◽  
Beatrice Barra ◽  
Sara Conti ◽  
Matthew Perich ◽  
Katie Zhuang ◽  
...  

Abstract Recovering arm control is a top priority for people with paralysis. Unfortunately, the complexity of the neural mechanisms underlying arm control practically limited the effectiveness of neurotechnology approaches. Here, we exploited the neural function of surviving spinal circuits to restore voluntary arm and hand control in three monkeys with spinal cord injury using spinal cord stimulation. Our neural interface leverages the functional organization of the dorsal roots to convey artificial excitation via electrical stimulation to relevant spinal segments at appropriate movement phases. Stimulation bursts, triggered by intracortical signals produced sustained arm movements enabling monkeys with arm paralysis to perform an unconstrained, three-dimensional reach-and-grasp task. Stimulation specifically improved strength, task performances and movement quality. Electrophysiology suggested that artificial recruitment of the sensory afferents was synergistically integrated with spared descending inputs and spinal reflexes to produce coordinated movements. The efficacy and reliability of our approach hold realistic promises of clinical translation.


2005 ◽  
Vol 94 (5) ◽  
pp. 3199-3210 ◽  
Author(s):  
E. Manjarrez ◽  
Z. Hernández-Paxtián ◽  
A. F. Kohn

Successive stimuli of constant intensity applied to Ia afferents produce spinal monosynaptic reflexes (MSRs) of variable amplitude. We recorded simultaneous MSRs in the left and right L7 (or L6) ventral roots of anesthetized cats. We analyzed the cross-covariance (CCV) between the amplitudes of bilateral MSRs. Long-time series (5 to 8 h) of these bilateral MSRs exhibited transitory changes in their covariations (as measured by the zero-lag peak of their CCV), thus suggesting the existence of certain neural sources contributing to produce these changes. The aim of the present study was to show that spinal centers producing negative spontaneous cord dorsum potentials (nSCDPs) contribute to maintain correlations in the amplitude of bilateral MSRs. After spinal cord transection at the L1 segment, no significant changes were observed in the correlation between the amplitude of bilateral nSCDPs versus the amplitude of bilateral MSRs. However, this correlation, as well as the peak at zero lag in the CCV between bilateral MSRs and the CCV between bilateral nSCDPs, respectively, were abolished after a subsequent longitudinal bisection at the L1–S2 spinal segments. These results suggest that lumbar spinal neurons (bilaterally interconnected) contribute to maintain the synchronous fluctuations of bilateral MSRs.


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