A small, computationally flexible network produces the phenotypic diversity of song recognition in crickets

Abstract

How neural networks evolved to generate the diversity of species-specific communication signals is unknown. For receivers of the signals one hypothesis is that novel recognition phenotypes arise from parameter variation in computationally flexible feature detection networks. We test this hypothesis in crickets, where males generate and females recognize the mating songs with a species-specific pulse pattern, by investigating whether the song recognition network in the cricket brain has the computational flexibility to recognize different temporal features. Using electrophysiological recordings from the network that recognizes crucial properties of the pulse pattern on the short timescale in the cricket Gryllus bimaculatus, we built a computational model that reproduces the neuronal and behavioral tuning of that species. An analysis of the models parameter space reveals that the network can provide all recognition phenotypes for pulse duration and pause known in crickets and even other insects. Phenotypic diversity in the model is consistent with known preference types in crickets and other insects, and arise from computations that likely evolved to increase energy efficiency and robustness of pattern recognition. The models parameter to phenotype mapping is degenerate--different network parameters can create similar changes in the phenotype--which likely supports evolutionary plasticity. Our study suggests that computationally flexible networks underlie the diverse pattern recognition phenotypes and we reveal network properties that constrain and support behavioral diversity.