Ruach, Rotem et al. (2019) International Worm Meeting "Irrational behavior in C. elegans arises due to asymmetric modulatory effects between options."

Eyal, Itskovits, Iwanir, Shachar, Ruach, Rotem, Pritz, Christian, Bokman, Eduard, Zaslaver, Alon

[International Worm Meeting, 2019]

Animals, like humans, repeatedly violate rational-choice paradigms, yet the underlying reasons remain debatable. This is primarily because population variability, past experience, current state, and future expectations affect decision-making cognitive processes, thus precluding decisive conclusions. Here, we established C. elegans nematodes as a powerful model for studying rationality of an innate behavior - chemotaxis, thus overcoming many of the above confounding effects. Moreover, innate behaviors presumably evolved to comply with rational economic axioms to maximize fitness. Surprisingly, we found that worms' chemotaxis behavior robustly violates key rationality paradigms of transitivity, independence of irrelevant alternatives and regularity. These violations arise due to asymmetric modulatory effects between the presented options. Functional analysis of the entire chemosensory system at a single-neuron resolution, coupled with analyses of mutants, defective in individual neurons, reveals that these asymmetric effects originate in specific sensory neurons. Thus, asymmetric modulations between options' representations may provide a simple explanation for irrational behavior.

Bokman, Eduard et al. (2019) International Worm Meeting "Encoding principles of a compact sensory system."

Ruach, Rotem, Zaslaver, Alon, Itskovits, Eyal, Bokman, Eduard, Pritz, Christian

[International Worm Meeting, 2019]

Animals critically depend on accurate sensation and processing of environmental cues. This task becomes particularly challenging for animals with a small and highly interconnected sensory system. Here, we used Caenorhabditis elegans nematodes to investigate how information is encoded within a compact sensory system. For this, we generated a new strain expressing the genetically encoded calcium indicator GCaMP in all 60 ciliated neurons, and used a fast-scanning confocal system to measure activity simultaneously from all chemosensory neurons while subjecting the worms to various stimuli. We found that the sensory system responds with small, unique, and mostly bi-laterally symmetrical subsets of neurons. Moreover, analysis of mutants, defective in neuro-transmitter or neuro-peptide release, revealed that the number of primary neurons, which directly respond to the cue, is minimal, typically comprised of 2-3 neuron types. Interestingly, these neurons exhibit a range of response dynamics that is both stimulus and circuitry-dependent, effectively increasing encoding capacity of the compact sensory system. Finally, exposing animals to combinations of stimuli revealed that the sensory system integrates information using a simple weighted sum strategy. These findings elucidate the principles that allow a small and compact sensory system to expand its encoding repertoire and to efficiently extract information from the environment.

Pritz, Christian et al. (2021) International Worm Meeting "Principles for coding associative memories in a compact neural network"

Itskovits, Eyal, Menasherof, Mai, Zaslaver, Alon, Nelken, Tal, Pritz, Christian, Ruach, Rotem, Bokman, Eduard, Gritsenko, Vladimir, Azulay, Aharon

[International Worm Meeting, 2021]

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 olfactory associative memories (short- and long-term memories, each as positive and negative associations) are encoded within the compact neural network of C. elegans worms. By combining these robust training paradigms with fast confocal calcium imaging using multi-neuron and whole-brain imaging approaches, we systematically traced experience-dependent activity changes down to the level of individual neurites. Interestingly, short-term, but not long-term, memory broadly altered memory-evoked responses of chemosensory neurons. Modulated activity in three neurons, namely AWA, AWC, and ASE, sufficed to discriminate between the different memory states. This economy in memory-coding neurons increases memory capacity and limits non-innate behavioral responses. In contrast, long-term memory was relegated to deeper layers of the network. Primary interneurons, AIY and AIA, exhibit memory-state-dependent activation signatures, allowing the sensory system to resume innate functionality. In conclusion, olfactory associative memory appears to follow a hierarchical and temporally structured encoding logic.