Location and function of serotonin in the central and peripheral nervous system of the Colorado potato beetle

T. van Haeften

Research output: Thesisinternal PhD, WU

Abstract

<p>In this thesis we have localized serotoninergic neurons in the central and peripheral nervous system of the Colorado potato beetle, <em>Leptinotarsa decemlineata</em> by means of immunohistochemistry with a specific antiserurn to serotonin and assessed the possible role of these neurons in feeding physiology. Emphasis was laid on the location of serotoninergic neurons involved in: (1) channelling of sensory information from antennal and gustatory sensory systems to the central nervous system; (2) the central organization of the serotoninergic neuron system providing information on possible central processing of this information; and the routes of innervation of possible target organs.<p>We have shown that about 200 serotoninergic neurons are present in the cerebral ganglion complex of the beetle, representing interneurons serving short- and long range communication. These neurons were grouped according to their location, number, and distribution of their processes. Clusters of paired protocerebral neurons appeared to be responsible for left-right communication within the brain and are the sole source of immunoreactivity in the central complex and the corpora pedunculata. Other neurons in the optic lobes and the deutocerebrum are likely to play an important role in the processing of visual and olfactory information respectively. This serotoninergic network in the brain does not project to other parts of the central nervous system and has the appearance of an individual serotoninergic neural unit. No neurons with a secretory function are present in the cerebral ganglion complex, nor are there structural indications that serotoninergic neurons are involved with the control of peptidergic neurosecretory neurons in the protocerebrum ( <strong>Chapter 2</strong> )<p>In the remainder of the central nervous system, the ventral nerve cord, altogether 74 serotoninergic neurons were found and their organization pattern enabled us to group them into five neuron classes. Two paired segmental twin interneurons are present in each ganglion or neuromere. These neurons have extensive dendritic arborizations in the contralateral hemisphere of the ganglion, and small arborization close to the perikaryon. Their axons take a contra- and ipsilateral course to more frontally and/ or caudally located ganglia. The distribution of processes is indicative of a division of labour among these neurons. The intersegmental projection are indicative of a function in interganglionic communication, whereas the dendritic projections suggest a function in the coordination of left-right neural activity within the ganglia. Four large frontal secretory neurons are present in the suboesophageal ganglion with axons projecting to a diffuse neurohemal system on oesophageal nerves. A pair of large caudal efferent neurons in the terminal ganglion send their processes in the proctodaeal nerves and innervate the proximal part of the hindgut. The function of miniature and terminal neurons is unknown. The distribution pattern of serotonin-like immunoreactivity enabled us to distinguish three separate putative functional units. The function of the caudal functional unit might be the synaptic control of caudal neurons innervating the alimentary canal, the function of the other two units is unknown ( <strong>Chapter 3</strong> ).<p>The presence of serotoninergic axons in the proctodaeal nerves indicated that the gut might be under serotoninergic control. By means of immunohistochemistry, it was shown that the alimentary canal of the beetle receives innnervation from two separate sources. Large efferent neurons in both the stomatogastric and central nervous system innervate the gut. Four neurons in the frontal ganglion have axons which run via the recurrent nerve to the circular and longitudinal muscles of the fore- and anterior midgut and supply the surface of these muscles with neurohemal axon swellings. The posterior midgut is devoid of immunoreactivity. The longitudinal muscles of the hindgut are supplied by the two caudal neurons described in <strong>Chapter 3</strong> . Electron-microscopical inspections of the axon swellings showed that exocytosis of immunolabelled vesicles occurs at some distance from the muscles fibres, indicating that the gut muscles might be under neurohormonal control. No serotoninergic synapses are observed on muscle fibres. A possible serotoninergic neurohormonal control of gut muscles, was confirmed in a bioassay. It appeared that administration of graded dosages of serotonin to the incubation medium has a clear inhibitory effect on spontaneous contractions of hindguts in vitro at concentrations of 10 <sup><font size="-2">-8</font></SUP>-10 <sup><font size="-2">-8</font></SUP>M. This effect was dose-dependent ( <strong>Chapter 4</strong> ).<p>Other organs might be under serotoninergic control as well. Two diffuse neurohemal systems for serotonin are present in the head of the beetle. Axons of four secretory neurons in the suboesophageal ganglion, described in <strong>Chapter 3</strong> , enter the ipsilateral mandibular nerve and cover the surface with a dense network of immunoreactive swellings. Two efferent neurons in the frontal ganglion have processes that run into the frontal connectives. Here, the axons emerge and form a similar network of axon swellings on the surface of the labro-frontal, pharyngeal, and antennal nerves, and on the frontal ganglion. Electron microscopy showed that these axon swellings are located outside the impermeable neural sheath, surrounding the nerves, and hence in close contact with the hemolymph. Next to this neurohemal release, a targeted release of serotonin occurs near the muscles of labrum, mandibles, pharynx, and salivary glands, indicating that these organs are under serotoninergic control ( <strong>Chapter 5</strong> ).<p>We have investigated the presence of serotoninergic sensory neuronal cell bodies in sensilla on labial and maxillary palps, galea, ventral labrum, tarsi, and compound eyes. It appeared that no afferent serotoninergic neurons are present in the peripheral nervous system of the beetle ( <strong>Chapter 6</strong> ).<p>The studies presented in this thesis show that the biogenic amine serotonin (5- hydroxytryptamine) is a ubiquitous and versatile neuroactive substance in both the central and peripheral nervous system of the Colorado potato beetle. In the central nervous system it is present in interneurons serving intra- and interganglionic communication. Here, it probably functions as a neurotransmitter and/or neuromodulator. A small number of serotoninergic neurons release serotonin, via elaborate ways, as a neurohormone into the hemolymph and/or close to their target organs.<p>In this thesis we have provided evidence that serotoninergic neurons are involved in the regulation of some aspects of feeding physiology at both the central and peripheral level. In the central nervous system, several serotoninergic interneurons, i.e. those in the cerebral ganglion complex, participate in the channelling and the central processing of antennal and optic information, whereas other interneurons, i.e. those in the ventral nerve cord, are part of functional neural units which are proposed to control efferent neurons, e.g. the caudal neurons innervating the hindgut. Serotoninergic neurosecretory neurons are involved in control of gut functioning, as shown in immunohistochemical and bioassay studies. Another class of efferent neurosecretory neurons were shown to innervate salivary glands and muscles of labrum, mandibles, and anterior pharynx, indicating that these organs might also be under serotoninergic control.
Original languageEnglish
QualificationDoctor of Philosophy
Awarding Institution
Supervisors/Advisors
  • Schoonhoven, L.M., Promotor, External person
  • Schooneveld, H., Promotor, External person
Award date23 Jun 1993
Place of PublicationHeteren
Publisher
Print ISBNs9789054851417
Publication statusPublished - 1993

Keywords

  • chrysomelidae
  • neuropeptides

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