Functional Circuitry Controlling the Selection of Behavioral Primitives in Caenorhabditis elegans
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One central question of neuroscience asks how a neural system can generate the diversity of complex behaviors needed to meet the range of possible demands placed on an organism by an ever changing environment. In many cases, it appears that animals assemble complex behaviors by recombining sets of simpler behaviors known as behavioral primitives. The crawling behavior of the nematode worm Caenorhabditis elegans represents a classic example of such an approach since worms use the simple behaviors of forward and reverse locomotion to assemble more complex behaviors such as search and escape. The relative simplicity and well-described anatomy of the worm nervous system combined with a high degree of genetic tractability make C. elegans an attractive organism with which to study the neural circuits responsible for assembling behavioral primitives into complex behaviors. Unfortunately, difficulty probing the physiological properties of central synapses in C. elegans has left this opportunity largely unfulfilled. In this dissertation we address this challenge by developing techniques that combine whole-cell patch clamp recordings with optical stimulation of neurons. We do this using transgenic worms that express the light-sensitive ion channel Channelrhodopsin-2 (ChR2) in putative pre-synaptic neurons and fluorescent protein reporters in the post-synaptic neurons to be targeted by electrodes. We first apply this new approach to probe C. elegans circuitry in chapter II where we test for connectivity between nociceptive neurons known as ASH required for sensing aversive stimuli, and premotor neurons required for generating backward locomotion, known as AVA. In chapter III we extend our analysis of the C. elegans locomotory circuit to the premotor neurons required for generating forward locomotion, known as AVB. We identify inhibitory synaptic connectivity between ASH and AVB and between the two types of premotor neurons, AVA and AVB. Finally, we use our observations to develop a biophysical model of the locomotory circuit in which switching emerges from the attractor dynamics of the network. Primitive selection in C. elegans may thus represent an accessible system to test kinetic theories of decision making. This dissertation includes previously published co-authored material.