A convergent and essential interneuron pathway for Mauthner-cell-mediated escapes.
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Abstract | The Mauthner cell (M-cell) is a command-like neuron in teleost fish whose firing in response to aversive stimuli is correlated with short-latency escapes [1-3]. M-cells have been proposed as evolutionary ancestors of startle response neurons of the mammalian reticular formation [4], and studies of this circuit have uncovered important principles in neurobiology that generalize to more complex vertebrate models [3]. The main excitatory input was thought to originate from multisensory afferents synapsing directly onto the M-cell dendrites [3]. Here, we describe an additional, convergent pathway that is essential for the M-cell-mediated startle behavior in larval zebrafish. It is composed of excitatory interneurons called spiral fiber neurons, which project to the M-cell axon hillock. By in vivo calcium imaging, we found that spiral fiber neurons are active in response to aversive stimuli capable of eliciting escapes. Like M-cell ablations, bilateral ablations of spiral fiber neurons largely eliminate short-latency escapes. Unilateral spiral fiber neuron ablations shift the directionality of escapes and indicate that spiral fiber neurons excite the M-cell in a lateralized manner. Their optogenetic activation increases the probability of short-latency escapes, supporting the notion that spiral fiber neurons help activate M-cell-mediated startle behavior. These results reveal that spiral fiber neurons are essential for the function of the M-cell in response to sensory cues and suggest that convergent excitatory inputs that differ in their input location and timing ensure reliable activation of the M-cell, a feedforward excitatory motif that may extend to other neural circuits. |
Year of Publication | 2015
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Journal | Curr Biol
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Volume | 25
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Issue | 11
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Pages | 1526-34
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Date Published | 2015 Jun 01
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ISSN | 1879-0445
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URL | |
DOI | 10.1016/j.cub.2015.04.025
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PubMed ID | 25959971
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PubMed Central ID | PMC4452389
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Grant list | R01 NS049319 / NS / NINDS NIH HHS / United States
K99 DC012775 / DC / NIDCD NIH HHS / United States
R01 GM085357 / GM / NIGMS NIH HHS / United States
R01 NS041886 / NS / NINDS NIH HHS / United States
T32 HL007901 / HL / NHLBI NIH HHS / United States
M01 RR002635 / RR / NCRR NIH HHS / United States
T32HL007901 / HL / NHLBI NIH HHS / United States
R01 HL109525 / HL / NHLBI NIH HHS / United States
R01HL109525 / HL / NHLBI NIH HHS / United States
R00 DC012775 / DC / NIDCD NIH HHS / United States
K99DC012775 / DC / NIDCD NIH HHS / United States
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