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Multiple excitatory and inhibitory neural signals converge to fine-tune Caenorhabditis elegans feeding to food availability

Multiple excitatory and inhibitory neural signals converge to fine-tune Caenorhabditis elegans feeding to food availability
Multiple excitatory and inhibitory neural signals converge to fine-tune Caenorhabditis elegans feeding to food availability
How an animal matches feeding to food availability is a key question for energy homeostasis. We addressed this in the nematode Caenorhabditis elegans, which couples feeding to the presence of its food (bacteria) by regulating pharyngeal activity (pumping). We scored pumping in the presence of food and over an extended time course of food deprivation in wild-type and mutant worms to determine the neural substrates of adaptive behavior. Removal of food initially suppressed pumping but after 2 h this was accompanied by intermittent periods of high activity. We show pumping is fine-tuned by context-specific neural mechanisms and highlight a key role for inhibitory glutamatergic and excitatory cholinergic/peptidergic drives in the absence of food. Additionally, the synaptic protein UNC-31 [calcium-activated protein for secretion (CAPS)] acts through an inhibitory pathway not explained by previously identified contributions of UNC-31/CAPS to neuropeptide or glutamate transmission. Pumping was unaffected by laser ablation of connectivity between the pharyngeal and central nervous system indicating signals are either humoral or intrinsic to the enteric system. This framework in which control is mediated through finely tuned excitatory and inhibitory drives resonates with mammalian hypothalamic control of feeding and suggests that fundamental regulation of this basic animal behavior may be conserved through evolution from nematode to humanavailability
behavioral plasticity, fasting, glutamate, neuropeptide, unc-31
0892-6638
836-848
Dalliere, N.
bcc4ebee-8955-4d7c-bed1-a5c13f4748f8
Bhatla, N.
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Luedtke, Z.
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Ma, D.K.
94c6861b-c164-4e72-b018-f2db9805adff
Woolman, J.
14e2a53e-94aa-47a5-8eab-eeb98ff5e3d4
Walker, R.
9368ac2d-f1e9-4bd9-a4b4-4a161c4aa140
Holden-Dye, L.
8032bf60-5db6-40cb-b71c-ddda9d212c8e
O'Connor, V.
8021b06c-01a0-4925-9dde-a61c8fe278ca
Dalliere, N.
bcc4ebee-8955-4d7c-bed1-a5c13f4748f8
Bhatla, N.
7f9f8ad0-8701-4bb4-8f03-4863bf698038
Luedtke, Z.
0d19fdb1-7db7-4c3a-9ad4-2534a52f86b5
Ma, D.K.
94c6861b-c164-4e72-b018-f2db9805adff
Woolman, J.
14e2a53e-94aa-47a5-8eab-eeb98ff5e3d4
Walker, R.
9368ac2d-f1e9-4bd9-a4b4-4a161c4aa140
Holden-Dye, L.
8032bf60-5db6-40cb-b71c-ddda9d212c8e
O'Connor, V.
8021b06c-01a0-4925-9dde-a61c8fe278ca

Dalliere, N., Bhatla, N., Luedtke, Z., Ma, D.K., Woolman, J., Walker, R., Holden-Dye, L. and O'Connor, V. (2016) Multiple excitatory and inhibitory neural signals converge to fine-tune Caenorhabditis elegans feeding to food availability. The FASEB Journal, 30 (2), 836-848. (doi:10.1096/fj.15-279257). (PMID:26514165)

Record type: Article

Abstract

How an animal matches feeding to food availability is a key question for energy homeostasis. We addressed this in the nematode Caenorhabditis elegans, which couples feeding to the presence of its food (bacteria) by regulating pharyngeal activity (pumping). We scored pumping in the presence of food and over an extended time course of food deprivation in wild-type and mutant worms to determine the neural substrates of adaptive behavior. Removal of food initially suppressed pumping but after 2 h this was accompanied by intermittent periods of high activity. We show pumping is fine-tuned by context-specific neural mechanisms and highlight a key role for inhibitory glutamatergic and excitatory cholinergic/peptidergic drives in the absence of food. Additionally, the synaptic protein UNC-31 [calcium-activated protein for secretion (CAPS)] acts through an inhibitory pathway not explained by previously identified contributions of UNC-31/CAPS to neuropeptide or glutamate transmission. Pumping was unaffected by laser ablation of connectivity between the pharyngeal and central nervous system indicating signals are either humoral or intrinsic to the enteric system. This framework in which control is mediated through finely tuned excitatory and inhibitory drives resonates with mammalian hypothalamic control of feeding and suggests that fundamental regulation of this basic animal behavior may be conserved through evolution from nematode to humanavailability

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Accepted/In Press date: 14 October 2015
e-pub ahead of print date: 29 October 2015
Published date: February 2016
Keywords: behavioral plasticity, fasting, glutamate, neuropeptide, unc-31
Organisations: Centre for Biological Sciences

Identifiers

Local EPrints ID: 383655
URI: http://eprints.soton.ac.uk/id/eprint/383655
ISSN: 0892-6638
PURE UUID: 472fb4cd-21b5-4d66-81a5-f257f73ac2f6
ORCID for R. Walker: ORCID iD orcid.org/0000-0002-9031-7671
ORCID for L. Holden-Dye: ORCID iD orcid.org/0000-0002-9704-1217

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Date deposited: 20 Nov 2015 10:33
Last modified: 10 Dec 2019 01:59

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