Morphological and Physiological Studies of a Stretch Receptor Neurone in the Leech, Hirudo medicinalis

Thompson, Stephen Wann Nicholas (1986) Morphological and Physiological Studies of a Stretch Receptor Neurone in the Leech, Hirudo medicinalis. PhD thesis, University of Glasgow.

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Abstract

This study gives the first description of an identified stretch receptor neurone in a soft bodied invertebrate. Intracellular recordings were made from the stretch receptor neurone (SRN), whose peripheral cell body and terminals lie in the ventral longitudinal muscle of the body wall of the medicinal leech, Hirudo medicinalis. Injection of depolarising current (3-4 nA) into the cell body elicited a large (40-70 mV) overshooting action potential. Paired intracellular recordings made from the cell body and its from its axon approximately 3-4 mm away as it enters the segmental ganglion showed that the action potential elicited in the soma is not actively propagated. Rather, inposed voltage changes are transmitted decrementally to the central nervous system, the axon being unable to support regenerative activity. The large length constant of the SRN (4.1 mm) and high specific membrane resistance (22.0 Kohm cm2) make the cell well adapted to conduct voltage changes over large distances with minimal decay of signal amplitude. Intracellular injection of the enzyme horseradish peroxidase (HRP) and the fluorescent dye Lucifer Yellow (LY) was used to study the morphology of the SRN. Two flat fan-shaped sensory terminals, approximately 70 um wide but only 2-3 microns deep are separated by a large (70 mum times 30 mum) cell body. A 10 um diameter axon runs centrally from the proximal fan shaped dendrite towards the CNS and at a distance of approximately 3-4 mm arborises within the ipsilateral half of the segmental ganglion in a characteristic branching pattern. The response of the neurone to changes in body wall length was studied by applying single ramp stretches or ramp releases to a thin strip of the ventral longitudinal muscle with which the SRN was associated whilst recording intracellularly from its axon as it enters the segmental ganglion. The cell responded to a ramp stretch stimulus with an electrotonically conducted hyperpolarising potential, maintained for the duration of the stretch. The neurone responded to a ramp release of the longitudinal muscle with an electrotonic depolarising potential. This consisted of an initial dynamic component followed by a lower amplitude static response which was maintained for the duration of the ramp stimulus. The responses of the cell to both a ramp release and ramp stretch were graded and proportional to the final amplitude of the stimulus. Stepped changes of body wall length resulted in concomitant stepped hyperpolarisation or depolarisation of the SRN membrane potential. Evidence is presented that the SRN responds to changes in longitudinal muscle tension rather than its absolute length. From observations on the tension changes which accompany natural changes in body wall posture and which occur during locomotory behaviours, it is apparent that tension changes during active contraction and relaxation of the dorsal and ventral longitudinal muscle are not those which are predicted from observation of the passive behaviour of the muscle during imposed stretches and ramp releases. The SRN is innervated by sensory neurones whose cell bodies are situated within the CNS. Paired intracellular recordings have shown that the SRN is post synaptic to three different modalities of primary sensory neurone. Action potentials arising in one of these mechanosensory neurones, the ipsilateral lateral nociceptive neurone, are followed on a 1:1 basis and with a constant latency by an excitatory post synaptic potential (epsp) in the peripheral cell body of the SRN. Action potentials elicited by direct depolarisation of all centrally situated ipsilateral touch and pressure mechanosensory neurone cell bodies also elicited epsp's in the SRN soma. No synaptic connectivity was recorded either between the ipsilateral medial nociceptive neurone and the SRN or any contralaterally sited mechanosensory neurones and the SRN. The central connections of the SRN with identified motoneurones to the longitudinal muscle of the body wall was investigated. Dual intracellular HRP injections showed that close apposition of SRN axon branches and dendrites from the large longitudinal motoneurone (L cell) occured within the ganglionic neuropile. Considerable overlap of the dendritic trees of motoneurones involved in the swimming rhythm and the SRN were also shown within the neuropile. Paired electrical recordings were made to investigate the effect of SRN activity upon motoneurone discharge. Imposed DC changes of the membrane potential of the ventral stretch receptor neurone did not produce any consistent modulation of the activity of individual identified motoneurones recorded either intracellularly from their centrally situated somata or extracellularly from their projecting axons. Preliminary experiments were carried out to determine the degree of coherence of motoneurone activity in the presence and absence of SRN input. When this method was applied to three simultaneous extracellular motoneurone spike trains the coherence of activity between any two motoneurones was only significant in the presence of the SRN input.

Item Type: Thesis (PhD)
Qualification Level: Doctoral
Keywords: Physiology, Neurosciences
Date of Award: 1986
Depositing User: Enlighten Team
Unique ID: glathesis:1986-77383
Copyright: Copyright of this thesis is held by the author.
Date Deposited: 14 Jan 2020 11:53
Last Modified: 14 Jan 2020 11:53
URI: http://theses.gla.ac.uk/id/eprint/77383

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