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Abstract:
A fundamental tenet of neuroscience is that nervous system function emerges from synaptic connectivity. How evolutionary modifications in behavior manifest themselves in the nervous system is poorly understood due to a paucity of system-level connectivity data. Predatory feeding in the nematode Pristionchus pacificus is an evolutionary novelty that increases the complexity of its behavioral palette. In the first comparison of its kind, we use thin-section TEM to compare synaptic connectivity in the pharyngeal nervous systems of P. pacificus with Caenorhabditis elegans to understand how the connectome evolves. We reveal homology between the nervous systems of P. pacificus and C. elegans, which are composed of identical sets of identified neurons that can generate very different behavioral output. Synaptic connectivity was found to be surprisingly divergent given the anatomical similarity. We identified the I1 and I2 interneurons as candidates for enabling differential regulation of pharyngeal muscle cells during predatory vs. bacterial feeding in P. pacificus. Changes in connectivity of the M5 motorneuron, which in C. elegans is presynaptic to the grinder muscle cells (pm7) are a neurobiological correlate to the loss of a grinder in P. pacificus. A system-level comparison in network topology reveals substantial shifts in nervous system architecture. In P. pacificus, the I4 interneuron is shown to be the only neuron in the pharynx that is not presynaptic to muscle cells, compared to 9 neurons in C. elegans. This suggests information flow is substantially different in the two species. Interestingly, I4 has much higher betweenness centrality in P. pacificus than in C. elegans. Various measures show pm4 (median bulb muscle cell), pm5 (isthmus muscle cell) and g1D (dorsal gland cell) to be the primary outputs of the system in both species. Using centrality measures and a force-directed graph analysis, we show that the C. elegans network focuses primarily on the isthmus, whereas the P. pacificus network focuses primarily on the median bulb. Previous work has shown that there are more classes of neurons expressing serotonin in P. pacificus than in C. elegans (Rivard et al., 2010). Consistent with these observations, eigenvector and PageRank centrality measures show a reduced role for NSM as an output of the system in P. pacificus. Our comparison has revealed the network architecture associated with evolutionary changes in behavior and yields testable hypotheses of network function in both P. pacificus and C. elegans.
