TY - JOUR
T1 - Signal diversification is associated with corollary discharge evolution in weakly electric fish
AU - Fukutomi, Matasaburo
AU - Carlson, Bruce A.
N1 - Funding Information:
Received Apr. 15, 2020; revised June 11, 2020; accepted July 6, 2020. Author contributions: M.F. and B.A.C. designed research; M.F. performed research; M.F. analyzed data; M.F. and B.A.C. wrote the paper. This work was supported by National Science Foundation Grant IOS-1755071 to B.A.C., and the Uehara Memorial Foundation to M.F. We thank Carl D. Hopkins and Natalie Trzcinski for kindly providing their Knollenorgan recording data; Adalee Lube for assistance with electrophysiology; and Erika Schumacher for assistance with statistical analysis. The authors declare no competing financial interests. Correspondence should be addressed to Bruce A. Carlson at [email protected]. https://doi.org/10.1523/JNEUROSCI.0875-20.2020 Copyright © 2020 the authors
Funding Information:
This work was supported by National Science Foundation Grant IOS-1755071 to B.A.C., and the Uehara Memorial Foundation to M.F. We thank Carl D. Hopkins and Natalie Trzcinski for kindly providing their Knollenorgan recording data; Adalee Lube for assistance with electrophysiology; and Erika Schumacher for assistance with statistical analysis.
Publisher Copyright:
© 2020 the authors
PY - 2020/8/12
Y1 - 2020/8/12
N2 - Communication signal diversification is a driving force in the evolution of sensory and motor systems. However, little is known about the evolution of sensorimotor integration. Mormyrid fishes generate stereotyped electric pulses (electric organ discharge [EOD]) for communication and active sensing. The EOD has diversified extensively, especially in duration, which varies across species from 0.1 to .10 ms. In the electrosensory hindbrain, a corollary discharge that signals the timing of EOD production provides brief, precisely timed inhibition that effectively blocks responses to self-generated EODs. However, corollary discharge inhibition has only been studied in a few species, all with short-duration EODs. Here, we asked how corollary discharge inhibition has coevolved with the diversification of EOD duration. We addressed this question by comparing 7 mormyrid species (both sexes) having varied EOD duration. For each individual fish, we measured EOD duration and then measured corollary discharge inhibition by recording evoked potentials from midbrain electrosensory nuclei. We found that delays in corollary discharge inhibition onset were strongly correlated with EOD duration as well as delay to the first peak of the EOD. In addition, we showed that electrosensory receptors respond to self-generated EODs with spikes occurring in a narrow time window immediately following the first peak of the EOD. Direct comparison of time courses between the EOD and corollary discharge inhibition revealed that the inhibition overlaps the first peak of the EOD. Our results suggest that internal delays have shifted the timing of corollary discharge inhibition to optimally block responses to self-generated signals.
AB - Communication signal diversification is a driving force in the evolution of sensory and motor systems. However, little is known about the evolution of sensorimotor integration. Mormyrid fishes generate stereotyped electric pulses (electric organ discharge [EOD]) for communication and active sensing. The EOD has diversified extensively, especially in duration, which varies across species from 0.1 to .10 ms. In the electrosensory hindbrain, a corollary discharge that signals the timing of EOD production provides brief, precisely timed inhibition that effectively blocks responses to self-generated EODs. However, corollary discharge inhibition has only been studied in a few species, all with short-duration EODs. Here, we asked how corollary discharge inhibition has coevolved with the diversification of EOD duration. We addressed this question by comparing 7 mormyrid species (both sexes) having varied EOD duration. For each individual fish, we measured EOD duration and then measured corollary discharge inhibition by recording evoked potentials from midbrain electrosensory nuclei. We found that delays in corollary discharge inhibition onset were strongly correlated with EOD duration as well as delay to the first peak of the EOD. In addition, we showed that electrosensory receptors respond to self-generated EODs with spikes occurring in a narrow time window immediately following the first peak of the EOD. Direct comparison of time courses between the EOD and corollary discharge inhibition revealed that the inhibition overlaps the first peak of the EOD. Our results suggest that internal delays have shifted the timing of corollary discharge inhibition to optimally block responses to self-generated signals.
KW - Animal communication
KW - Electrosensory system
KW - Evolution
KW - Sensorimotor integration
KW - Sensory coding
UR - http://www.scopus.com/inward/record.url?scp=85089411279&partnerID=8YFLogxK
U2 - 10.1523/JNEUROSCI.087520.2020
DO - 10.1523/JNEUROSCI.087520.2020
M3 - Article
C2 - 32661026
AN - SCOPUS:85089411279
SN - 0270-6474
VL - 40
SP - 6345
EP - 6356
JO - Journal of Neuroscience
JF - Journal of Neuroscience
IS - 33
ER -