Behavioral variation correlates with differences in single neuron serotonin receptor subtype expression within and across species

The marine mollusc, Pleurobranchaea californica varies daily in whether it swims and this correlates with whether serotonin (5-HT) enhances the strength of synapses made by the swim central pattern generator neuron, C2. Another species, Tritonia diomedea, reliably swims and does not vary in serotonergic neuromodulation. A third species, Hermissenda crassicornis, never produces this behavior and lacks the neuromodulation. We found that expression of particular 5-HT receptor genes in C2 correlates with swimming. Seven 5-HT receptor subtype genes were identified from whole-brain transcriptomes. We isolated individual C2 neurons and sequenced their RNA or measured 5-HT receptor gene expression using quantitative PCR. C2 neurons isolated from Pleurobranchaea individuals that produced a swim motor pattern just prior to isolation expressed the 5-HT2a and 5-HT7 receptor genes, as did the Tritonia samples. These subtypes were absent from C2 neurons isolated from Pleurobranchaea individuals that did not swim that day and from Hermissenda C2 neurons. Expression of other receptors did not correlate with swimming. This suggests that 5-HT2a and 5-HT7 receptors mediate the modulation of C2 synaptic strength and play an important role in swimming. Furthermore, the results suggest that regulation of receptor expression might underlie daily changes in behavior as well as behavioral evolution.