PUBLICATION

Behavioral role of the reciprocal inhibition between a pair of Mauthner cells during fast escapes in zebrafish

Authors
Shimazaki, T., Tanimoto, M., Oda, Y., Higashijima, S.I.
ID
ZDB-PUB-181224-13
Date
2018
Source
The Journal of neuroscience : the official journal of the Society for Neuroscience   39(7): 1182-1194 (Journal)
Registered Authors
Higashijima, Shin-ichi, Oda, Yoichi
Keywords
none
MeSH Terms
  • Acoustic Stimulation
  • Animals
  • Animals, Genetically Modified
  • Escape Reaction/physiology*
  • Excitatory Postsynaptic Potentials/physiology
  • Interneurons/physiology
  • Larva
  • Neural Pathways/cytology*
  • Neural Pathways/physiology*
  • Neurons/physiology*
  • Psychomotor Performance/physiology
  • Rhombencephalon/cytology*
  • Rhombencephalon/physiology*
  • Spinal Cord/cytology*
  • Spinal Cord/physiology*
  • Zebrafish/physiology*
PubMed
30578342 Full text @ J. Neurosci.
Abstract
During many behaviors in vertebrates, the central nervous system (CNS) generates asymmetric activities between the left and right sides to produce asymmetric body movements. For asymmetrical activations of the CNS, reciprocal inhibition between the left and right sides is believed to play a key role. However, the complexity of the CNS makes it difficult to identify the reciprocal inhibition circuits at the level of individual cells and the contribution of each neuron to the asymmetric activity. Using larval zebrafish, we examined this issue by investigating reciprocal inhibition circuits between a pair of Mauthner (M) cells, giant reticulospinal neurons that trigger fast escapes. Previous studies have shown that a class of excitatory neurons, called cranial relay neurons (CRNs), is involved in the reciprocal inhibition pathway between the M-cells. Using transgenic fish, in which two of the CRNs (Ta1 and Ta2) expressed GFP, we showed that Ta1 and Ta2 constitute major parts of the pathway. In larvae in which Ta1/Ta2 were laser-ablated, the amplitude of the reciprocal IPSPs dropped to less than one-third. Calcium imaging and electrophysiological recording showed that the occurrence probability of bilateral M-cell activation upon sound/vibration stimuli was greatly increased in the Ta1/Ta2-ablated larvae. Behavioral experiments revealed that the Ta1/Ta2 ablation resulted in shallower body bends during sound/vibration-evoked escapes, which is consistent with the observation that increased occurrence of bilateral M-cell activation impaired escape performance. Our study revealed major components of the reciprocal inhibition circuits in the M-cell system and the behavioral importance of the circuits.Significance StatementsReciprocal inhibition between the left and right side of the CNS is considered imperative for producing asymmetric movements in animals. It has been difficult, however, to identify the circuits at the individual cell level and their role in behavior. Here, we address this problem by examining the reciprocal inhibition circuits of the hindbrain Mauthner (M) cell system in larval zebrafish. We determined that two paired interneurons play a critical role in the reciprocal inhibition between the paired M-cells and that the reciprocal inhibition prevents bilateral firing of the M-cells and is thus necessary for the full body-bend during M-cell-initiated escape. Further, we discussed the cooperation of multiple reciprocal inhibitions working in the hindbrain and spinal cord to ensure high-performance escapes.
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Human Disease / Model
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Fish
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