Variations on a theme: species differences in synaptic connectivity do not predict central pattern generator activity.

A fundamental question in comparative neuroethology is the extent to which synaptic wiring determines behavior vs. the extent to which it is constrained by phylogeny. We investigated this by examining the connectivity and activity of homologous neurons in different species. and (Mollusca, Gastropoda, Nudibranchia) have homologous neurons and exhibit homologous swimming behaviors consisting of alternating left-right (LR) whole body flexions. Yet, a homologous interneuron (Si1) differs between the two species in its participation in the swim motor pattern (SMP) and synaptic connectivity. In this study we examined Si1 homologs in two additional nudibranchs: , which evolved LR swimming independently of and , and , which swims with dorsal-ventral (DV) body flexions. In , the contralateral Si1s exhibit alternating rhythmic bursting activity during the SMP and are members of the swim central pattern generator (CPG), as in The Si1 homologs in do not burst rhythmically during the DV SMP but are inhibited and receive bilaterally synchronous synaptic input. In both and , the Si1 homologs exhibit reciprocal inhibition, as in However, in the inhibition is polysynaptic, whereas in it is monosynaptic, as in In all species, the contralateral Si1s are electrically coupled. These results suggest that and convergently evolved a swim CPG that contains Si1; however, they differ in monosynaptic connections. Connectivity is more similar between and , which exhibit different swimming behaviors. Thus connectivity between homologous neurons varies independently of both behavior and phylogeny. This research shows that the synaptic connectivity between homologous neurons exhibits species-specific variations on a basic theme. The neurons vary in the extent of electrical coupling and reciprocal inhibition. They also exhibit different patterns of activity during rhythmic motor behaviors that are not predicted by their circuitry. The circuitry does not map onto the phylogeny in a predictable fashion either. Thus neither neuronal homology nor species behavior is predictive of neural circuit connectivity.