Cellular Mechanisms of Cortisol-Induced Changes in Mauthner-Cell Excitability in the Startle Circuit of Goldfish

Predator pressure and olfactory cues (alarm substance) have been shown to modulate Mauthner cell (M-cell) initiated startle escape responses (C-starts) in teleost fish. The regulation of such adaptive responses to potential threats is thought to involve the release of steroid hormones such as cortis...

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Main Authors: Daniel R. Bronson, Thomas Preuss
Format: Article
Language:English
Published: Frontiers Media S.A. 2017-09-01
Series:Frontiers in Neural Circuits
Subjects:
Online Access:http://journal.frontiersin.org/article/10.3389/fncir.2017.00068/full
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author Daniel R. Bronson
Thomas Preuss
author_facet Daniel R. Bronson
Thomas Preuss
author_sort Daniel R. Bronson
collection DOAJ
description Predator pressure and olfactory cues (alarm substance) have been shown to modulate Mauthner cell (M-cell) initiated startle escape responses (C-starts) in teleost fish. The regulation of such adaptive responses to potential threats is thought to involve the release of steroid hormones such as cortisol. However, the mechanism by which cortisol may regulate M-cell excitability is not known. Here, we used intrasomatic, in vivo recordings to elucidate the acute effects of cortisol on M-cell membrane properties and sound evoked post-synaptic potentials (PSPs). Cortisol tonically decreased threshold current in the M-cell within 10 min before trending towards baseline excitability over an hour later, which may indicate the involvement of non-genomic mechanisms. Consistently, current ramp injection experiments showed that cortisol increased M-cell input resistance in the depolarizing membrane, i.e., by a voltage-dependent postsynaptic mechanism. Cortisol also increases the magnitude of sound-evoked M-cell PSPs by reducing the efficacy of local feedforward inhibition (FFI). Interestingly, another pre-synaptic inhibitory network mediating prepulse inhibition (PPI) remained unaffected. Together, our results suggest that cortisol rapidly increases M-cell excitability via a post-synaptic effector mechanism, likely a chloride conductance, which, in combination with its dampening effect on FFI, will modulate information processing to reach threshold. Given the central role of the M-cell in initiating startle, these results are consistent with a role of cortisol in mediating the expression of a vital behavior.
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spelling doaj.art-a8b7d3adad1e44ea891426fad925fbd12022-12-22T03:46:18ZengFrontiers Media S.A.Frontiers in Neural Circuits1662-51102017-09-011110.3389/fncir.2017.00068293773Cellular Mechanisms of Cortisol-Induced Changes in Mauthner-Cell Excitability in the Startle Circuit of GoldfishDaniel R. Bronson0Thomas Preuss1The Graduate Center, City University of New York, New York, NY, United StatesHunter College, City University of New York, New York, NY, United StatesPredator pressure and olfactory cues (alarm substance) have been shown to modulate Mauthner cell (M-cell) initiated startle escape responses (C-starts) in teleost fish. The regulation of such adaptive responses to potential threats is thought to involve the release of steroid hormones such as cortisol. However, the mechanism by which cortisol may regulate M-cell excitability is not known. Here, we used intrasomatic, in vivo recordings to elucidate the acute effects of cortisol on M-cell membrane properties and sound evoked post-synaptic potentials (PSPs). Cortisol tonically decreased threshold current in the M-cell within 10 min before trending towards baseline excitability over an hour later, which may indicate the involvement of non-genomic mechanisms. Consistently, current ramp injection experiments showed that cortisol increased M-cell input resistance in the depolarizing membrane, i.e., by a voltage-dependent postsynaptic mechanism. Cortisol also increases the magnitude of sound-evoked M-cell PSPs by reducing the efficacy of local feedforward inhibition (FFI). Interestingly, another pre-synaptic inhibitory network mediating prepulse inhibition (PPI) remained unaffected. Together, our results suggest that cortisol rapidly increases M-cell excitability via a post-synaptic effector mechanism, likely a chloride conductance, which, in combination with its dampening effect on FFI, will modulate information processing to reach threshold. Given the central role of the M-cell in initiating startle, these results are consistent with a role of cortisol in mediating the expression of a vital behavior.http://journal.frontiersin.org/article/10.3389/fncir.2017.00068/fullcortisolMauthner-cellin vivo electrophysiologyhormonesinput resistancevoltage-gated ion channels
spellingShingle Daniel R. Bronson
Thomas Preuss
Cellular Mechanisms of Cortisol-Induced Changes in Mauthner-Cell Excitability in the Startle Circuit of Goldfish
Frontiers in Neural Circuits
cortisol
Mauthner-cell
in vivo electrophysiology
hormones
input resistance
voltage-gated ion channels
title Cellular Mechanisms of Cortisol-Induced Changes in Mauthner-Cell Excitability in the Startle Circuit of Goldfish
title_full Cellular Mechanisms of Cortisol-Induced Changes in Mauthner-Cell Excitability in the Startle Circuit of Goldfish
title_fullStr Cellular Mechanisms of Cortisol-Induced Changes in Mauthner-Cell Excitability in the Startle Circuit of Goldfish
title_full_unstemmed Cellular Mechanisms of Cortisol-Induced Changes in Mauthner-Cell Excitability in the Startle Circuit of Goldfish
title_short Cellular Mechanisms of Cortisol-Induced Changes in Mauthner-Cell Excitability in the Startle Circuit of Goldfish
title_sort cellular mechanisms of cortisol induced changes in mauthner cell excitability in the startle circuit of goldfish
topic cortisol
Mauthner-cell
in vivo electrophysiology
hormones
input resistance
voltage-gated ion channels
url http://journal.frontiersin.org/article/10.3389/fncir.2017.00068/full
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