Direct activation of the Mauthner cell by electric field pulses drives ultrarapid escape responses.
Rapid escape swims in fish are initiated by the Mauthner cells, giant reticulospinal neurons with unique specializations for swift responses. The Mauthner cells directly activate motoneurons and facilitate predator detection by integrating acoustic, mechanosensory, and visual stimuli. In addition, larval fish show well-coordinated escape responses when exposed to electric field pulses (EFPs). Sensitization of the Mauthner cell by genetic overexpression of the voltage-gated sodium channel SCN5 increased EFP responsiveness, whereas Mauthner ablation with an engineered variant of nitroreductase with increased activity (epNTR) eliminated the response. The reaction time to EFPs is extremely short, with many responses initiated within 2 ms of the EFP. Large neurons, such as Mauthner cells, show heightened sensitivity to extracellular voltage gradients. We therefore tested whether the rapid response to EFPs was due to direct activation of the Mauthner cells, bypassing delays imposed by stimulus detection and transmission by sensory cells. Consistent with this, calcium imaging indicated that EFPs robustly activated the Mauthner cell but only rarely fired other reticulospinal neurons. Further supporting this idea, pharmacological blockade of synaptic transmission in zebrafish did not affect Mauthner cell activity in response to EFPs. Moreover, Mauthner cells transgenically expressing a tetrodotoxin (TTX)-resistant voltage-gated sodium channel retained responses to EFPs despite TTX suppression of action potentials in the rest of the brain. We propose that EFPs directly activate Mauthner cells because of their large size, thereby driving ultrarapid escape responses in fish.
Program in Genomics of Differentiation, Eunice Kennedy Shriver National Institute of Child Health and Human Development, Bethesda, Maryland;
Kathryn M
KM
Tabor
Program in Genomics of Differentiation, Eunice Kennedy Shriver National Institute of Child Health and Human Development, Bethesda, Maryland;
Sadie A
SA
Bergeron
Program in Genomics of Differentiation, Eunice Kennedy Shriver National Institute of Child Health and Human Development, Bethesda, Maryland;
Eric J
EJ
Horstick
Program in Genomics of Differentiation, Eunice Kennedy Shriver National Institute of Child Health and Human Development, Bethesda, Maryland;
Diana C
DC
Jordan
Institute of Biomedicine, University of Helsinki, Helsinki, Finland; and.
Vilma
V
Aho
Institute of Biomedicine, University of Helsinki, Helsinki, Finland; and.
Tarja
T
Porkka-Heiskanen
Department of Biological Sciences, New Jersey Institute of Technology, Newark, New Jersey.
Gal
G
Haspel
Program in Genomics of Differentiation, Eunice Kennedy Shriver National Institute of Child Health and Human Development, Bethesda, Maryland; burgessha@mail.nih.gov.
Harold A
HA
Burgess
D000200:Action Potentials; D000818:Animals; D002118:Calcium / Q000378:metabolism; D060126:Characidae; D003530:Cyprinidae; D004558:Electric Stimulation; D062554:NAV1.5 Voltage-Gated Sodium Channel / Q000235:genetics / Q000378:metabolism; D009474:Neurons / Q000378:metabolism / Q000502:physiology*; D009990:Oryzias; D011930:Reaction Time; D012249:Rhombencephalon / Q000166:cytology / Q000502:physiology; D026941:Sodium Channel Blockers / Q000494:pharmacology; D013550:Swimming; D009435:Synaptic Transmission; D013779:Tetrodotoxin / Q000494:pharmacology; D015027:Zebrafish
D062554:NAV1.5 Voltage-Gated Sodium Channel; D026941:Sodium Channel Blockers; D013779:Tetrodotoxin; D002118:Calcium
Mauthner cell; SCN5; electric pulse; escape response; nitroreductase