Spatiotemporal transition in the role of synaptic inhibition to the tail beat rhythm of developing larval zebrafish
Open accessAbstract
Significant maturation of swimming in zebrafish (Danio rerio) occurs within the first few days of life when fish transition from coiling movements to burst swimming and then to beat-and-glide swimming. This maturation occurs against a backdrop of numerous developmental changes - neurogenesis, a transition from predominantly electrical to chemical-based neurotransmission, and refinement of intrinsic properties. There is evidence that spinal locomotor circuits undergo fundamental changes as the zebrafish transitions from burst to beat-and-glide swimming. Our electrophysiological recordings confirm that the operation of spinal locomotor circuits becomes increasingly reliant on glycinergic neurotransmission for rhythmogenesis governing the rhythm of tail beats. This transition occurred at the same time that we observed a change in rhythmicity of synaptic inhibition to spinal motoneurons (MNs). When we examined whether the transition from weakly to strongly glycinergic dependent rhythmogenesis occurred at a uniform pace across the length of the spinal cord, we found that this transition occurred earlier at caudal segments than at rostral segments of the spinal cord. Furthermore, while this rhythmogenic transition occurred when fish transition from burst swimming to beat-and-glide swimming, these two transitions were not interdependent. These results suggest that there is a developmental transition in the operation of spinal locomotor circuits that is gradually set in place in the spinal cord in a caudo-rostral temporal sequence.
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Spinal circuits transitioned from relying upon pacemakers with endogenous bursting properties during coiling toward depending upon network oscillators whose rhythm is driven by excitatory and inhibitory synapses.
“Specifically, we demonstrated that spinal circuits transitioned from relying upon pacemakers with endogenous bursting properties during coiling toward depending upon network oscillators whose rhythm is driven by excitatory and inhibitory synapses (Roussel et al., 2020).”
From Modeling spinal locomotor circuits for movements in developing zebrafish (2021) · cites this paper as Roussel et al., 2020
The Results section (‘Modelling a change in rhythmogenesis’) supports a developmental shift from endogenously bursting pacemakers to network oscillators that rely on glycinergic inhibition; the Discussion also describes this as a model-supported interpretation. The passages do not establish that excitatory synapses drive the later rhythm, and ‘demonstrated’ is stronger than the paper’s ‘suggest’ and ‘potentially’ language. No page numbers are available in our copy. (LLM, conf=0.86)
Experimental — accuracy not yet measuredThe transition from coiling to swimming involves a delegation of rhythm generation from ICs to spinal locomotor circuits.
“This capacity suggests that the transition from coiling to swimming involves a delegation of rhythm generation from ICs to spinal locomotor circuits (Roussel et al., 2020).”
From Modeling spinal locomotor circuits for movements in developing zebrafish (2021) · cites this paper as Roussel et al., 2020
The Results (Figure 8 and its accompanying text; page unavailable) propose a shift from IC pacemakers before 3 days postfertilization to spinal network oscillators later in development. But the paper places that proposed shift during the change from burst swimming to beat-and-glide swimming, not specifically at the transition from coiling to swimming. (LLM, conf=0.86)
Experimental — accuracy not yet measuredThe maturation from coiling to later stages of swimming is accompanied by an operational switch in how spinal locomotor circuits generate the rhythm underlying tail beats.
“We have recently provided evidence that the maturation from coiling to later stages of swimming is accompanied by an operational switch in how spinal locomotor circuits generate the rhythm underlying tail beats.”
From Modeling spinal locomotor circuits for movements in developing zebrafish (2021) · cites this paper as Roussel et al., 2020
Experimental evidence from the authors' lab suggests that a transition from a rhythm driven by a pacemaker kernel to a rhythm driven by local network oscillators occurs progressively from the caudal toward the rostral end of the body.
“Experimental evidence from our lab further suggests that a transition from a rhythm driven by a pacemaker kernel to a rhythm driven by local network oscillators occurs progressively from the caudal toward the rostral end of the body (Roussel et al., 2020).”
From Modeling spinal locomotor circuits for movements in developing zebrafish (2021) · cites this paper as Roussel et al., 2020
Previous experimental results showed that strychnine application disturbed swimming in the 20-40 Hz range at later stages of development.
“Previous experimental results showed that strychnine application disturbed swimming in the 20–40 Hz range at later stages of development (Roussel et al., 2020).”
From Modeling spinal locomotor circuits for movements in developing zebrafish (2021) · cites this paper as Roussel et al., 2020
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Modeling spinal locomotor circuits for movements in developing zebrafish
Roussel, Y., Gaudreau, S. F., Kacer, E. R., Sengupta, M., & Bui, T. V. (2021) · eLife · doi:10.7554/elife.67453 · Cited by 39 · see citing works
Self-citationComputational modeling of speed microcircuits in larval zebrafish spinal cord with <i>Sili</i> Fish
Topcu, E., & Bui, T. V. (2025) · Journal of Neurophysiology · doi:10.1152/jn.00393.2024
Self-citation
- Authors
- Roussel, Y., Paradis, M., Gaudreau, S. F., Lindsey, B. W., & Bui, T. V.
- Affiliations
- University of Ottawa (CA)
- Corresponding author
- Bui, Tuan V.
- Venue
- eneuro
- Publisher
- Society for Neuroscience
- Published
- 2020-01
- Volume
- 7
- Issue
- 1
- Pages
- ENEURO.0508-18.2020
- ISSN
- 2373-2822 (ISSN-L)
- PMC
- PMC7029186
- OpenAlex
- W3003192070
- Cited by
- 14
- References
- 4
- Citations by year
- 2026: 2 · 2025: 6 · 2024: 1 · 2022: 2 · 2021: 2 · 2020: 1
- FWCI
- 0.62
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- eNeuro (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Funders
- Gouvernement du Canada | Natural Sciences and Engineering Research Council of Canada (RGPIN-2015-06403)
- Gouvernement du Canada | Canadian Institutes of Health Research (MFE-158137)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Zebrafish Biomedical Research Applications
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Keywords
- synaptic inhibition, glycinergic neurotransmission, spinal locomotor circuits, zebrafish larvae, burst swimming, spinal motoneurons, rhythmogenesis
- MeSH terms
- Animals, Larva, Locomotion, Motor Neurons, Spinal Cord, Swimming, Zebrafish
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