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Nitric oxide synthase in crayfish walking leg ganglia: Segmental differences in chemo-tactile centers argue against a generic role in sensory integration

Nitric oxide synthase in crayfish walking leg ganglia: Segmental differences in chemo-tactile centers argue against a generic role in sensory integration
Nitric oxide synthase in crayfish walking leg ganglia: Segmental differences in chemo-tactile centers argue against a generic role in sensory integration
Nitric oxide (NO) is a diffusible signaling molecule with evolutionarily conserved roles in neural plasticity. Prominent expression of NO synthase (NOS) in the primary olfactory centers of mammals and insects lead to the notion of a special role for NO in olfaction. In insects, however, NOS is also strongly expressed in non-olfactory chemo-tactile centers of the thoracic nerve cord. The functional significance of this apparent association with various sensory centers is unclear, as is the extent to which it occurs in other arthropods. We therefore investigated the expression of NOS in the pereopod ganglia of crayfish (Pacifastacus lenisculus and Procambarus clarkii). Conventional NADPH diaphorase (NADPHd) staining after formaldehyde fixation gave poor anatomic detail, whereas fixation in methanol/formalin (MF-NADPHd) resulted in Golgi-like staining, which was supported by immunohistochemistry using NOS antibodies that recognize a 135-kDa protein in crayfish. MF-NADPHd revealed an exceedingly dense innervation of the chemo-tactile centers. As in insects, this innervation was provided by a system of prominent intersegmental neurons. Superimposed on a putatively conserved architecture, however, were pronounced segmental differences. Strong expression occurred only in the anterior three pereopod ganglia, correlating with the presence of claws on pereopods one to three. These clawed pereopods, in addition to their role in locomotion, are crucially involved in feeding, where they serve both sensory and motor functions. Our findings indicate that strong expression of NOS is not a universal feature of primary sensory centers but instead may subserve a specific requirement for sensory plasticity that arises only in particular behavioral contexts.
crustacean nervous system, NADPH diaphorase histochemistry, immunohistochemistry, olfaction, gustation
0021-9967
381-399
Ott, S.R.
7fac3995-eca9-41a1-ac09-9944f7fd5137
Aonuma, H.
97d3511a-fc4f-4246-a86f-cd927a3356b4
Newland, P.L.
7a018c0e-37ba-40f5-bbf6-49ab0f299dbb
Elphick, M.R.
493866d6-0503-43d3-90f3-c9b9aa1cbd86
Ott, S.R.
7fac3995-eca9-41a1-ac09-9944f7fd5137
Aonuma, H.
97d3511a-fc4f-4246-a86f-cd927a3356b4
Newland, P.L.
7a018c0e-37ba-40f5-bbf6-49ab0f299dbb
Elphick, M.R.
493866d6-0503-43d3-90f3-c9b9aa1cbd86

Ott, S.R., Aonuma, H., Newland, P.L. and Elphick, M.R. (2007) Nitric oxide synthase in crayfish walking leg ganglia: Segmental differences in chemo-tactile centers argue against a generic role in sensory integration. Journal of Comparative Neurology, 501 (3), 381-399. (doi:10.1002/cne.21242).

Record type: Article

Abstract

Nitric oxide (NO) is a diffusible signaling molecule with evolutionarily conserved roles in neural plasticity. Prominent expression of NO synthase (NOS) in the primary olfactory centers of mammals and insects lead to the notion of a special role for NO in olfaction. In insects, however, NOS is also strongly expressed in non-olfactory chemo-tactile centers of the thoracic nerve cord. The functional significance of this apparent association with various sensory centers is unclear, as is the extent to which it occurs in other arthropods. We therefore investigated the expression of NOS in the pereopod ganglia of crayfish (Pacifastacus lenisculus and Procambarus clarkii). Conventional NADPH diaphorase (NADPHd) staining after formaldehyde fixation gave poor anatomic detail, whereas fixation in methanol/formalin (MF-NADPHd) resulted in Golgi-like staining, which was supported by immunohistochemistry using NOS antibodies that recognize a 135-kDa protein in crayfish. MF-NADPHd revealed an exceedingly dense innervation of the chemo-tactile centers. As in insects, this innervation was provided by a system of prominent intersegmental neurons. Superimposed on a putatively conserved architecture, however, were pronounced segmental differences. Strong expression occurred only in the anterior three pereopod ganglia, correlating with the presence of claws on pereopods one to three. These clawed pereopods, in addition to their role in locomotion, are crucially involved in feeding, where they serve both sensory and motor functions. Our findings indicate that strong expression of NOS is not a universal feature of primary sensory centers but instead may subserve a specific requirement for sensory plasticity that arises only in particular behavioral contexts.

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More information

Submitted date: 13 July 2006
Published date: 1 March 2007
Keywords: crustacean nervous system, NADPH diaphorase histochemistry, immunohistochemistry, olfaction, gustation

Identifiers

Local EPrints ID: 56581
URI: http://eprints.soton.ac.uk/id/eprint/56581
ISSN: 0021-9967
PURE UUID: 3e5aaf4c-4963-40de-8853-e4d8e1bcf131
ORCID for P.L. Newland: ORCID iD orcid.org/0000-0003-4124-8507

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Date deposited: 08 Aug 2008
Last modified: 16 Mar 2024 02:59

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Contributors

Author: S.R. Ott
Author: H. Aonuma
Author: P.L. Newland ORCID iD
Author: M.R. Elphick

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