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Multiple excitatory and inhibitory neural signals converge to fine‐tune Caenorhabditis elegans feeding to food availability
Author(s) -
Dallière Nicolas,
Bhatla Nikhil,
Luedtke Zara,
Ma Dengke K.,
Woolman Jonathan,
Walker Robert J.,
HoldenDye Lindy,
O'Connor Vincent
Publication year - 2016
Publication title -
the faseb journal
Language(s) - English
Resource type - Journals
SCImago Journal Rank - 1.709
H-Index - 277
eISSN - 1530-6860
pISSN - 0892-6638
DOI - 10.1096/fj.15-279257
Subject(s) - excitatory postsynaptic potential , inhibitory postsynaptic potential , caenorhabditis elegans , glutamatergic , biology , neuroscience , context (archaeology) , glutamate receptor , microbiology and biotechnology , biochemistry , gene , paleontology , receptor
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 human.—Dallière, N., Bhatla, N., Luedtke, Z., Ma, D. K., Woolman, J., Walker, R. J., Holden‐Dye, L., O'Connor, V. Multiple excitatory and inhibitory neural signals converge to fine‐tune Caenorhabditis elegans feeding to food availability. FASEB J. 30, 836–848 (2016). www.fasebj.org