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9-Phenanthrol modulates postinhibitory rebound and afterhyperpolarizing potentials in an excitatory motor neuron of the medicinal leech

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Abstract

Postinhibitory rebound (PIR) responses in leech dorsal excitatory motor neurons (cell DE-3) are eliminated by Ca2+ channel blockers but also exhibit a strong dependence on extracellular Na+. These features could be explained by a voltage-gated Ca2+ current acting in concert with a Ca2+-activated nonspecific current (ICAN). In vertebrates, ICAN is associated with TRPM4 channels which are blocked selectively by 9-phenanthrol. Here, we show that 9-phenanthrol selectively inhibits a late phase of PIR and simultaneously enhances afterhyperpolarizing potentials (AHPs). Bath application of NNC 55-0396 or Cd2+ combined with ion substitution experiments indicate that a low-voltage-activated Ca2+ current plays a key role in generating PIR and that Ca2+ influx through low- or high-voltage-activated Ca2+ channels can trigger AHPs via activation of a Ca2+-dependent K+ current. We also demonstrate modulation of rebound responses by other ICAN blockers such as gadolinium and flufenamic acid, as well as the calmodulin antagonist W-7. We discuss how these results provide additional insights into the specific types of ionic currents underlying rebound responses of motor neuron DE-3 in the medicinal leech.

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Abbreviations

AHP:

Afterhyperpolarization

BAPTA:

1,2-Bis(o-aminophenoxy)ethane-N,N,N′,N′-tetraacetic acid

BK:

Big or large conductance subtype of K(Ca) channels

CAM:

Calmodulin

DE-3:

Dorsal excitatory motor neuron 3

DMSO:

Dimethyl sulfoxide

FFA:

Flufenamic acid

HVA:

High-voltage activated

ICa :

Voltage-gated Ca2+ current

ICAN :

Ca2+-activated nonspecific current

IKCa :

Ca2+-activated K+ current

IK:

Intermediate conductance subtype of K(Ca) channels

INaP :

Persistent Na+ current

K(Ca):

Calcium-activated potassium

Kir :

Inward rectifier

LVA:

Low-voltage activated

NNC:

NNC 55-0396

PIR:

Postinhibitory rebound

SK:

Small conductance subtype of K(Ca) channels

TRPM4:

Transient receptor potential ion channel (melastatin related, member 4)

V m :

Membrane potential

W-7:

N-(6-aminohexyl)-5-Chloro-1-naphthalene-sulfonamide hydrochloride

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Acknowledgements

This work was made possible by generous support from Siena College, including a Summer Scholars Research Fellowship to JRG. The authors thank Nicole Nocera for preliminary experiments using W-7 and Matthew Rebel for his assistance. All experiments are in accordance with current laws on animal experimentation and care in the USA.

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Authors and Affiliations

  1. Department of Biology, Siena College, Loudonville, NY, USA

    James D. Angstadt

  2. NYIT College of Osteopathic Medicine, Old Westbury, NY, USA

    Joshua R. Giordano

  3. University of New England College of Osteopathic Medicine, Biddeford, ME, USA

    Alexander J. Goncalves

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  1. James D. Angstadt
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Correspondence to James D. Angstadt.

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Angstadt, J.D., Giordano, J.R. & Goncalves, A.J. 9-Phenanthrol modulates postinhibitory rebound and afterhyperpolarizing potentials in an excitatory motor neuron of the medicinal leech. J Comp Physiol A 203, 613–633 (2017). https://doi.org/10.1007/s00359-017-1178-4

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