Neuronal plasticity regulated by the insulin-like signaling pathway underlies salt chemotaxis learning inCaenorhabditis elegans

Abstract

Oda S, Tomioka M, Iino Y. Neuronal plasticity regulated by the insulin-like signaling pathway underlies salt chemotaxis learning in Caenorhabditis elegans. J Neurophysiol 106: 301-308, 2011. First published April 27, 2011 doi:10.1152/jn.01029.2010.-Quantification of neuronal plasticity in a living animal is essential for understanding learning and memory. Caenorhabditis elegans shows a chemotactic behavior toward NaCl. However, it learns to avoid NaCl after prolonged exposure to NaCl under starvation conditions, which is called salt chemotaxis learning. Insulin-like signaling is important for this behavioral plasticity and functions in one of the salt-sensing sensory neurons, ASE right (ASER). However, how neurons including ASER show neuronal plasticity is unknown. To determine the neuronal plasticity related to salt chemotaxis learning, we measured Ca 2ϩ response and synaptic release of individual neurons by using in vivo imaging techniques. We found that response of ASER increased whereas its synaptic release decreased after prolonged exposure to NaCl without food. These changes in the opposite directions were abolished in insulin-like signaling mutants, suggesting that insulinlike signaling regulates these plasticities in ASER. The response of one of the downstream interneurons, AIB, decreased profoundly after NaCl conditioning. This alteration in AIB response was independent of the insulin-like signaling pathway. Our results suggest that information on NaCl is modulated at the level of both sensory neurons and interneurons in salt chemotaxis learning. learning and memory; in vivo imaging LEARNING AND MEMORY ARE CRUCIAL for animals to cope with a constantly changing environment. Previous studies suggested that insulin is involved in learning and memory in mammals (Dou et al. 2005; Zhao et al. 1999). Indeed, studies using mammalian cultured neurons or Xenopus tadpoles suggested that insulin regulates neuronal plasticities such as long-term depression (LTD), internalization of DL-␣-amino-3-hydroxy-5-methylisoxazole-propionic acid (AMPA) receptors, and changes in the number of synapses (Chiu et al. 2008;Man et al. 2000). However, how insulin actually regulates learning and memory is still obscure.Caenorhabditis elegans also shows learning and memory such as thermotaxis learning, food-odor associative learning, and salt chemotaxis learning (Mori et al. 2007;Nuttley et al. 2002; Saeki et al. 2001;Tomioka et al. 2006). The molecular mechanisms underlying these behavioral plasticities have been studied well. Insulin-like signaling, for instance, regulates several types of starvation-associated learning (Kodama et al. 2006;Lin et al. 2010;Tomioka et al. 2006). However, the plasticities of neuronal activity underlying these behavioral plasticities are mostly unknown.Salt chemotaxis learning is one of the starvation-associated learning types. In this behavioral plasticity, worms show aversive behavior toward the attractant NaCl after prolonged exposure to NaCl for 10 -60 min without food. However, in the presence of f...

Environmental CO 2 inhibits Caenorhabditis elegans egg-laying by modulating olfactory neurons and evokes widespread changes in neural activity

“…Many of the CO 2 -responsive neurons we have identified, including ASE, ASH, ASK, ADL, and AWC, make synaptic connection onto the AIA interneurons. Previous studies suggest AWC, ASH, and ASK inhibit AIA (32, 33) whereas ASEL inputs probably are excitatory (34). A rise in CO 2 evoked a rise in AIA Ca 2+ , consistent with excitatory input (Fig.…”

Multiple Sensory Inputs Are Extensively Integrated to Modulate Nociception in C. elegans

“…To stimulate ASEL activity with a salt up-step, animals were incubated on NGM plates and transferred to NGM (50 mM NaCl) plates ϩ10 mM NaCl for 10 min and 1-octanol avoidance assayed after 2 min, as described above. To stimulate ASER activity with a salt down-step, animals were transferred to NGM plates ϩ10 mM NaCl for 10 min and then transferred to NGM plates and 1-octanol avoidance was assayed after 2 min, as described above (Suzuki et al, 2008;Oda et al, 2011). The rate of spontaneous reversal was assayed on and off food, as described previously (Gray et al, 2005).…”

“…For electrophysiology, animals either had an AIB cell body exposed with a small incision in the cuticle using standard protocols (Goodman et al, 1998;Piggott et al, 2011) or were more fully dissected with a second incision longitudinally on the contralateral side to expose the entirety of the AIB interneurons to the drug-containing solution. Glutamate was applied as described above.…”

“…C. elegans, with 14 pairs of sensory neurons and complex, sensory-mediated locomotory behaviors, provides an excellent model with which to study contextdependent multisensory interactions. For example, nociception and aversive responses mediated by the two ASH sensory neurons can be initiated through two distinct circuits, each of which is modulated independently to direct locomotory decision making (Piggott et al, 2011). Sensory-evoked aversive responses can be initiated by activation of the two AVA backward command interneurons directly and/or signaling from the AIB/RIM circuit that antagonizes forward locomotion (Piggott et al, 2011).…”

“…For example, nociception and aversive responses mediated by the two ASH sensory neurons can be initiated through two distinct circuits, each of which is modulated independently to direct locomotory decision making (Piggott et al, 2011). Sensory-evoked aversive responses can be initiated by activation of the two AVA backward command interneurons directly and/or signaling from the AIB/RIM circuit that antagonizes forward locomotion (Piggott et al, 2011). Indeed, ASH glutamatergic signaling is essential to initiate reversal in response to an array of noxious ligands (Mellem et al, 2002;Chao et al, 2004;Guo et al, 2009;Lindsay et al, 2011).…”