Highlights d Mice, like humans, perceive forepaw warming (R1 C) and discriminate warm from cool d Warm-activated and warm-silenced polymodal C-fibers both signal forepaw warming d Mice lacking the cool-sensitive ion channel TRPM8 are unable to perceive warm d The inability to perceive warm is associated with loss of warm-silenced C-fibers

In many communication systems, information is encoded in the temporal pattern of signals. For rhythmic signals that carry information in specific frequency bands, a neuronal system may profit from tuning its inherent filtering properties towards a peak sensitivity in the respective frequency range. The cricket Gryllus bimaculatus evaluates acoustic communication signals of both conspecifics and predators. The song signals of conspecifics exhibit a characteristic pulse pattern that contains only a narrow range of modulation frequencies. We examined individual neurons (AN1, AN2, ON1) in the peripheral auditory system of the cricket for tuning towards specific modulation frequencies by assessing their firing-rate resonance. Acoustic stimuli with a swept-frequency envelope allowed an efficient characterization of the cells' modulation transfer functions. Some of the examined cells exhibited tuned band-pass properties. Using simple computational models, we demonstrate how different, cell-intrinsic or network-based mechanisms such as subthreshold resonances, spike-triggered adaptation, as well as an interplay of excitation and inhibition can account for the experimentally observed firing-rate resonances. Therefore, basic neuronal mechanisms that share negative feedback as a common theme may contribute to selectivity in the peripheral auditory pathway of crickets that is designed towards mate recognition and predator avoidance.

Sensory systems process stimuli that greatly vary in intensity and complexity. To maintain efficient information transmission, neural systems need to adjust their properties to these different sensory contexts, yielding adaptive or stimulus-dependent codes. Here, we demonstrated adaptive spectrotemporal tuning in a small neural network, i.e. the peripheral auditory system of the cricket. We found that tuning of cricket auditory neurons was sharper for complex multi-band than for simple single-band stimuli. Information theoretical considerations revealed that this sharpening improved information transmission by separating the neural representations of individual stimulus components. A network model inspired by the structure of the cricket auditory system suggested two putative mechanisms underlying this adaptive tuning: a saturating peripheral nonlinearity could change the spectral tuning, whereas broad feed-forward inhibition was able to reproduce the observed adaptive sharpening of temporal tuning. Our study revealed a surprisingly dynamic code usually found in more complex nervous systems and suggested that stimulus-dependent codes could be implemented using common neural computations.

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