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Modulation of swimming behavior in the medicinal leech

III. Control of cellular properties in motor neurons by serotonin

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Abstract

Expression of swimming in the medicinal leech (Hirudo medicinalis) is modulated by serotonin, a naturally occurring neurohormone. Exogenous application of serotonin engenders ‘spontaneous’ swimming activity in nerve-cord preparations. We examined whether this activity is due to enhanced participation of swim motor neurons (MNs) in generating the swimming rhythm. We found that depolarizing current injections into MNs during fictive swimming are more effective in shifting cycle phase in nerve cords following serotonin exposure. In such preparations, the dynamics of membrane potential excursions following current injection into neuronal somata are substantially altered. We observed: 1) a delayed outward rectification (‘relaxation’) during depolarizing current injection, most marked in inhibitory MNs; and 2) in excitor MNs, an enhancement of postinhibitory rebound (PIR) and afterhyperpolarizing potentials (AHPs) following hyperpolarizing and depolarizing current pulses, respectively. In contrast, we found little alteration in MN properties in leech nerve cords depleted of amines. We propose that enhanced expression of swimming activity in leeches exposed to elevated serotonin is due, partly, to enhancement of relaxation, PIR and AHP in MNs. We believe that as a consequence of alterations in cellular properties and synaptic interactions (subsequent paper) by serotonin, MNs are reconfigured to more effectively participate in generating and expressing the leech swimming rhythm.

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Abbreviations

AHP :

Afterhyperpolarizing potential

DCC :

Discontinuous current clamp

DE :

Dorsal excitor motor neuron

DI :

Dorsal inhibitor motor neuron

IPSP :

Inhibitory postsynaptic potential

MN :

Motor neuron

PIR :

Postinhibitory rebound

VE :

Ventral excitor motor neuron

VI :

Ventral inhibitor motor neuron

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Author notes

  1. P. S. Mangan

    Present address: Department of Neurology, University of Virginia, Health Sciences Center, 22908, Charlottesville, VA, USA

Authors and Affiliations

  1. Department of Biology and NSF Center for Biological Timing, University of Virginia, 22901, Charlottesville, VA, USA

    P. S. Mangan, G. A. Curran, C. A. Hurney & W. O. Friesen

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  1. P. S. Mangan
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  2. G. A. Curran
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  3. C. A. Hurney
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  4. W. O. Friesen
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Mangan, P.S., Curran, G.A., Hurney, C.A. et al. Modulation of swimming behavior in the medicinal leech. J Comp Physiol A 175, 709–722 (1994). https://doi.org/10.1007/BF00191843

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