CONDITIONED DENDRITIC OSCILLATORS IN A LOBSTER MECHANORECEPTOR NEURON

Citation
D. Combes et al., CONDITIONED DENDRITIC OSCILLATORS IN A LOBSTER MECHANORECEPTOR NEURON, Journal of physiology, 499(1), 1997, pp. 161-177
Citations number
43
Categorie Soggetti
Physiology
Journal title
ISSN journal
00223751
Volume
499
Issue
1
Year of publication
1997
Pages
161 - 177
Database
ISI
SICI code
0022-3751(1997)499:1<161:CDOIAL>2.0.ZU;2-E
Abstract
1. Intra- and extracellular recordings were made from in vitro prepara tions of the lobster (Homarus gammarus) stomatogastric nervous system to study the nature and origin of pacemaker-like activity in a primary mechanoreceptor neurone, the anterior gastric receptor (AGR), whose t wo bilateral stretch sensitive dendrites ramify in the tendon of power stroke muscle GM1 of the gastric mill system. 2. Although the AGR is k nown to be autoactive, we report here that in 20% of our preparations, rather than autogenic tonic discharge, the receptor fired spontaneous ly in discrete bursts comprising three to ten action potentials and re peating at cycle frequencies of 0.5-2.5 Hz in the absence of mechanica l stimulation. Intrasomatic recordings revealed that such rhythmic bur sting was driven by slow oscillations in membrane potential, the frequ ency of which was voltage sensitive and dependent upon the level of st retch applied to the receptor terminals of the AGR. 3. Autoactive burs ting of the AGR originated from an endogenous oscillatory mechanism in the sensory dendrites themselves, since (i) during both steady: repet itive firing and bursting, somatic and axonal impulses were always pre ceded 1:1 by dendritic action potentials, (ii) hyperpolarizing the AGR cell body to block triggering of axonal impulses revealed attenuated somatic spikes that continued to originate from the two peripheral den drites, (iii) the timing of burst firing could be phase reset by brief electrical stimulation of either dendrite, and (iv) spontaneous burst ing continued to be expressed by an AGR dendrite after physical isolat ion from the GM1 muscle and the stomatogastric nervous system. 4. Alth ough a given AGR in, vitro could switch spontaneously from dendritic b ursting to tonic firing and vice versa, exogenous application of micro molar (or less) concentrations of the neuropeptide F1 (TNRNFLRFamide) to the dendritic membrane could rapidly and reversibly switch the rece ptor firing pattern from repetitive firing to the bursting mode. Expos ure of the somatic and axonal membrane of the AGR to F1 was without ef fect, as were applications of other neuroactive substances such as ser otonin, octopamine and proctolin. 5. We conclude that, as for many osc illatory neurones of the central nervous system, the intrinsic activit y pattern of this peripheral sensory neurone may be dynamically confer red by extrinsic modulatory influences, presumably according to comput ational demands. Moreover, the ability of the AGR to behave as an endo genous burster imparts considerable integrative complexity since, in t his activity mode, sensory coding not only occurs through the frequenc y modulation of on-going dendritic bursts but also via changes in the duration of individual bursts and their inherent spike frequencies.