Mechanisms underlying the recruitment of inhibitory interneurons in fictive swimming in developing Xenopus laevis tadpoles
| Autor: | Andrea Ferrario, Valentina Saccomanno, Hong-Yan Zhang, Roman Borisyuk, Wen-Chang Li |
|---|---|
| Přispěvatelé: | BBSRC, University of St Andrews. School of Psychology and Neuroscience, University of St Andrews. Institute of Behavioural and Neural Sciences |
| Jazyk: | angličtina |
| Rok vydání: | 2023 |
| Předmět: |
spinal-cord
Spinal postnatal-development spinal Integration integration interneuron Interneuron pattern generator excitatory interneurons electrophysiological properties swimming Swimming vesicle pools MCC larval zebrafish General Neuroscience intrinsic-properties Modeling modeling 3rd-DAS recruitment RC0321 locomotor rhythm Recruitment RC0321 Neuroscience. Biological psychiatry. Neuropsychiatry brain-stem |
| Popis: | Developing spinal circuits generate patterned motor outputs while many neurons with high membrane resistances are still maturing. In the spinal cord of hatchling frog tadpoles of unknown sex, we found that the firing reliability in swimming of inhibitory interneurons with commissural and ipsilateral ascending axons was negatively correlated with their cellular membrane resistance. Further analyses showed that neurons with higher resistances had outward rectifying properties, low firing thresholds, and little delay in firing evoked by current injections. Input synaptic currents these neurons received during swimming, either compound, unitary current amplitudes, or unitary synaptic current numbers, were scaled with their membrane resistances, but their own synaptic outputs were correlated with membrane resistances of their postsynaptic partners. Analyses of neuronal dendritic and axonal lengths and their activities in swimming and cellular input resistances did not reveal a clear correlation pattern. Incorporating these electrical and synaptic properties into a computer swimming model produced robust swimming rhythms, whereas randomizing input synaptic strengths led to the breakdown of swimming rhythms, coupled with less synchronized spiking in the inhibitory interneurons. We conclude that the recruitment of these developing interneurons in swimming can be predicted by cellular input resistances, but the order is opposite to the motor-strength-based recruitment scheme depicted by Henneman’s size principle. This form of recruitment/integration order in development before the emergence of refined motor control is progressive potentially with neuronal acquisition of mature electrical and synaptic properties, among which the scaling of input synaptic strengths with cellular input resistance plays a critical role.SIGNIFICANCE STATEMENTThe mechanisms on how interneurons are recruited to participate in circuit function in developing neuronal systems are rarely investigated. In 2-d-old frog tadpole spinal cord, we found the recruitment of inhibitory interneurons in swimming is inversely correlated with cellular input resistances, opposite to the motor-strength-based recruitment order depicted by Henneman’s size principle. Further analyses showed the amplitude of synaptic inputs that neurons received during swimming was inversely correlated with cellular input resistances. Randomizing/reversing the relation between input synaptic strengths and membrane resistances in modeling broke down swimming rhythms. Therefore, the recruitment or integration of these interneurons is conditional on the acquisition of several electrical and synaptic properties including the scaling of input synaptic strengths with cellular input resistances. |
| Databáze: | OpenAIRE |
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