A major goal in neuroscience is to elucidate the principles by which memories are stored in a neural network. Here, we have systematically studied how four types of associative memories (short- and long-term memories, each as positive and negative associations) are encoded within the compact neural network of Caenorhabditis elegans worms. Interestingly, sensory neurons were primarily involved in coding short-term, but not long-term, memories, and individual sensory neurons could be assigned to coding either the conditioned stimulus or the experience valence (or both). Moreover, when considering the collective activity of the sensory neurons, the specific training experiences could be decoded. Interneurons integrated the modulated sensory inputs and a simple linear combination model identified the experience-specific modulated communication routes. The widely distributed memory suggests that integrated network plasticity, rather than changes to individual neurons, underlies the fine behavioral plasticity. This comprehensive study reveals basic memory-coding principles and highlights the central roles of sensory neurons in memory formation. 

Principles for coding associative memories in a compact neural network

Memory is one of the most important abilities of the brain. It is defined as an alteration in behavior as a consequence of an experience. For example, the C. elegans nematode will downregulate its chemotactic response to the innately attractive odor, butanone, if the odor is not paired with food. Through repeated, spaced training with this odor in the absence of food, C. elegans will maintain this memory for a prolonged period of time. Although transient receptor potential (TRP) channels are classically thought of as primary sensory receptors, it was reported that the OSM-9/TRPV5/TRPV6 (TRP vanilloid 5/6) channel is required for single exposure learning. Here we describe a new role for osm-9 in consolidation of memory that is induced by repeated, spaced training. In this paradigm, osm-9 mutant animals learn as well as wild-types, but are unable to consolidate the memory. Though sleep is required for memory consolidation, loss of the TRPV channel OSM-9 does not affect sleep. This indicates that the TRP channel promotes memory in a process that acts outside the sleep pathway. We investigate the endogenous expression pattern of OSM-9 and show that it is not expressed in the butanone-responsive AWC olfactory sensory neuron. Instead, it is expressed in the paired AWA olfactory neuron, the ASH nociceptive neurons, the OLQ and two other unidentified sensory neurons which are most likely ADF and ADL as they express osm-9 mRNA. Because OSM-9 acts in sensory neurons that do not participate in butanone sensation, this indicates that the circuit participates in olfactory memory consolidation.

https://www.biorxiv.org/content/biorxiv/early/2020/12/12/2020.11.27.400747.full.pdf

Olfactory memory consolidation requires the TRPV channel OSM-9 in sensory neurons of the circuit.

Memory is one of the most important abilities of the brain. It is defined as an alteration in behavior from an experience. For example, the C. elegans nematode will downregulate its chemotactic response to an innately attractive odor if it is not paired with food. This process is an example of olfactory classical conditioning. Through spaced training with this odor in the absence of food, C. elegans will maintain this memory of the odor for a prolonged period of time, akin to long-term memory formation. Although TRP channels are classically thought of as primary sensory receptors, intriguingly, it has been reported that the OSM-9/TRPV5/TRPV6 (TRP vanilloid) channel is required for odor short-term memory. We have discovered a new role for osm-9/TRPV in long-term olfactory memory formation (LTM). The osm-9 mutant animals can acquire memory of the conditioned stimulus (odor) just like wild-type, but are unable to consolidate the memory for long-term maintenance. Interestingly, this TRPV-mediated long-term memory does not require sleep to form the long-lasting memory. Additionally, we found that genomic DNA and not cDNA is able to rescue the short-term odor memory defects seen in the null mutants. TRP channels are well studied in their ability to sense noxious stimuli, yet they are also implicated in memory and many diseases and disorders that limit neural plasticity, including Parkinsons disease, Alzheimers disease, stroke, and sense disorders including anosmia. Our studies uncovered a role of TRP channels in neural plasticity, specifically, in olfactory long-term memory formation. These findings will broaden our knowledge of TRP channel function as a mediator of plasticity and memory, which could also potentially aid in understanding and treating the many diseases and disorders caused by TRP channel dysfunction.

/pdf/the-trpv-channel-osm-9-mediates-olfactory-long-term-memory-2xub5gl9ow.pdf

The Trpv Channel Osm-9 Mediates Olfactory Long-Term Memory Consolidation Independent Of Sleep

While astrocytes are known to be important for development and nourishment of the nervous system, the field is just beginning to explore how astrocytes respond to environmental stimuli. Using Caenorhabditis elegans and their astrocyte-equivalent, CEPsh, we asked whether astrocyte-like glia respond to odor exposure. We found one day-old adult C. elegans decrease hlh-17 promoter (CEPsh glia marker) mediated fluorescent expression when trained with an innately attractive odor butanone. Moreover, the olfactory training paradigm itself affects phlh-17 expression, but in a different way. This suggests astrocyte-like CEPsh glia can integrate environmental information to respond to changes in the environment, which enhances survival.

/pdf/astrocyte-like-cepsh-glia-respond-to-stress-1bh9wlxb.pdf

Astrocyte-like CEPsh glia respond to stress

A major goal in neuroscience is to elucidate the principles by which memories are stored in a neural network Here, we have systematically studied how the four types of associative memories (short- and long-term memories, each formed using positive and negative associations) are encoded within the compact neural network of C elegans worms Interestingly, short-term, but not long-term, memories are evident in the sensory system Long-term memories are relegated to inner layers of the network, allowing the sensory system to resume innate functionality Furthermore, a small set of sensory neurons is allocated for coding short-term memories, a design that can increase memory capacity and limit non-innate behavioral responses Notably, individual sensory neurons may code for the conditioned stimulus or the experience valence Interneurons integrate these information to modulate animal behavior upon memory reactivation This comprehensive study reveals basic principles by which memories are encoded within a neural network, and highlights the central roles of sensory neurons in memory formation

/pdf/principles-for-coding-associative-memories-in-a-compact-3qa2jonalv.pdf

Summary Sleep is conserved across phyla and is shown here to be required for memory consolidation in the nematode, C. elegans. However, it is unclear how sleep collaborates with experience to change specific neurons and associated synapses to ultimately affect behavior. C. elegans neurons have defined synaptic connections and described contributions to specific behaviors. We show that spaced odor-training induces long-term memory, which transits a labile period before being stably maintained. This post-training labile period is required for long-term memory. Memory consolidation, but not acquisition, requires a single interneuron, AIY, which plays a role in odor-seeking behavior. We find that sleep and conditioning mark inhibitory synaptic connections between the butanone-sensing AWC neuron and AIY to decrease synapses and it is in the post-sleep wake phase that memory-specific synaptic changes occur. Thus, we demonstrate in the living organism how sleep initiates events lasting beyond the period of sleep to drive memory consolidation.

/pdf/sleep-is-required-for-odor-exposure-to-consolidate-memory-1uhzkv0kfp.pdf

Sleep is required for odor exposure to consolidate memory and remodel synapses

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Sleep is required for odor exposure to consolidate memory and remodel synapses