Conditional dendritic oscillators in a lobster mechanoreceptor neurone.
The Journal of Physiology. 1997-02-15; 499(1): 161-177
DOI: 10.1113/jphysiol.1997.sp021918
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Combes D(1), Simmers J, Moulins M.
Author information:
(1)Laboratoire de Neurobiologie et Physiologie Comparées, Université de Bordeaux I et CNRS, URA 1126, Arcachon, France.
1. Intra- and extracellular recordings were made from in vitro preparations 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 two bilateral stretch-sensitive dendrites
ramify in the tendon of powerstroke muscle GM1 of the gastric mill system. 2.
Although the AGR is known to be autoactive, we report here that in 20% of our
preparations, rather than autogenic tonic discharge, the receptor fired
spontaneously in discrete bursts comprising three to ten action potentials and
repeating at cycle frequencies of 0.5-2.5 Hz in the absence of mechanical
stimulation. Intrasomatic recordings revealed that such rhythmic bursting was
driven by slow oscillations in membrane potential, the frequency of which was
voltage sensitive and dependent upon the level of stretch applied to the
receptor terminals of the AGR. 3. Autoactive bursting of the AGR originated from
an endogenous oscillatory mechanism in the sensory dendrites themselves, since
(i) during both steady, repetitive firing and bursting, somatic and axonal
impulses were always preceded 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 dendrites, (iii) the timing of burst firing could be phase reset by
brief electrical stimulation of either dendrite, and (iv) spontaneous bursting
continued to be expressed by an AGR dendrite after physical isolation from the
GM1 muscle and the stomatogastric nervous system. 4. Although a given AGR in
vitro could switch spontaneously from dendritic bursting to tonic firing and
vice versa, exogenous application of micromolar (or less) concentrations of the
neuropeptide F1 (TNRNFLRFamide) to the dendritic membrane could rapidly and
reversibly switch the receptor firing pattern from repetitive firing to the
bursting mode. Exposure of the somatic and axonal membrane of the AGR to F1 was
without effect, as were applications of other neuroactive substances such as
serotonin, octopamine and proctolin. 5. We conclude that, as for many
oscillatory neurones of the central nervous system, the intrinsic activity
pattern of this peripheral sensory neurone may be dynamically conferred by
extrinsic modulatory influences, presumably according to computational demands.
Moreover, the ability of the AGR to behave as an endogenous burster imparts
considerable integrative complexity since, in this activity mode, sensory coding
not only occurs through the frequency modulation of on-going dendritic bursts
but also via changes in the duration of individual bursts and their inherent
spike frequencies.