Reliability of an interneuron response depends on an integrated sensory state

Abstract

The central nervous system transforms sensory information into representations that are salient to the animal. Here we define the logic of this transformation in a Caenorhabditis elegans integrating interneuron. AIA interneurons receive input from multiple chemosensory neurons that detect attractive odors. We show that reliable AIA responses require the coincidence of two sensory inputs: activation of AWA olfactory neurons that are activated by attractive odors, and inhibition of one or more chemosensory neurons that are inhibited by attractive odors. AWA activates AIA through an electrical synapse, while the disinhibitory pathway acts through glutamatergic chemical synapses. AIA interneurons have bistable electrophysiological properties consistent with their calcium dynamics, suggesting that AIA activation is a stereotyped response to an integrated stimulus. Our results indicate that AIA interneurons combine sensory information using AND-gate logic, requiring coordinated activity from multiple chemosensory neurons. We propose that AIA encodes positive valence based on an integrated sensory state.

Chemosensory signal transduction inCaenorhabditis elegans

“…Because ASK activation promotes reversals ( Wakabayashi et al 2004 ; Gray et al 2005 ), suppression of calcium signaling by a chemoattractant and activation by a chemorepellent could both contribute to appropriate behavioral responses and locomotion strategies in complex chemosensory environments. For example, calcium imaging revealed that inhibition of ASK by the addition of diacetyl contributes to the disinhibition of the downstream interneuron AIA, allowing AIA to more reliably respond to diacetyl-evoked depolarization of AWA ( Dobosiewicz et al 2019 ). While the application of E. coli supernatant decreases ASK calcium levels, an elevation (OFF response) was seen upon its removal ( Zaslaver et al 2015 ).…”

“…The AWA olfactory neuron pair senses bacterially produced volatile cues to direct animals toward potential food sources ( Bargmann et al 1993 ; Larsch et al 2013 ; Choi et al 2016 ; Worthy et al 2018a ; Dobosiewicz et al 2019 ; Table 1 ). However, there are sex differences in attraction to some odorants, including diacetyl ( Lee and Portman 2007 ; White et al 2007 ; Ryan et al 2014 ; Barr et al 2018 ).…”

“…AWA is an ON neuron that shows an elevated calcium levels in response to increases in diacetyl, pyrazine, 2-methylpyrazine, 2,4,5-trimethylthiazole and hexyl acetate ( Shinkai et al 2011 ; Larsch et al 2013 , 2015 ; Zaslaver et al 2015 ; Itskovits et al 2018 ; Liu et al 2018a ; Dobosiewicz et al 2019 ). This neuron pair also shows an increase in calcium in response to the addition of E. coli supernatant, and a decrease in calcium upon its removal ( Zaslaver et al 2015 ).…”

“…Thus, to model robust climbing of a gradient at higher odor concentrations, the spiking ON neuron pair had to be complemented with OFF neurons that had graded responses ( Itskovits et al 2018 ). The AWC neurons, with their response to intermediate concentrations of diacetyl, may fulfill this role ( Dobosiewicz et al 2019 ).…”

Principles for coding associative memories in a compact neural network

“…We identified two interneurons, AIA and RIA, whose activity was modulated in a stimulusand valence-specific manner, both following short-and long-term learning. The AIA interneurons are postsynaptic to most of the chemosensory neurons (White et al , 1986;Cook et al , 2019) , and had been shown to integrate various chemosensory inputs (Shinkai et al , 2011;Larsch et al , 2015;Dobosiewicz, Liu and Bargmann, 2019) . While AIA activity promotes forward locomotion (Garrity et al , 2010) , we found that long-term aversive training increased AIA activity together with increase in reversal rates (Fig.…”