The cellular coding of temperature in the mammalian cortex.

Temperature is a fundamental sensory modality separate from touch, with dedicated receptor channels and primary afferent neurons for cool and warm1-3. Unlike for other modalities, however, the cortical encoding of temperature remains unknown, with very few cortical neurons reported that respond to non-painful temperature, and the presence of a 'thermal cortex' is debated4-8. Here, using widefield and two-photon calcium imaging in the mouse forepaw system, we identify cortical neurons that respond to cooling and/or warming with distinct spatial and temporal response properties. We observed a representation of cool, but not warm, in the primary somatosensory cortex, but cool and warm in the posterior insular cortex (pIC). The representation of thermal information in pIC is robust and somatotopically arranged, and reversible manipulations show a profound impact on thermal perception. Despite being positioned along the same one-dimensional sensory axis, the encoding of cool and that of warm are distinct, both in highly and broadly tuned neurons. Together, our results show that pIC contains the primary cortical representation of skin temperature and may help explain how the thermal system generates sensations of cool and warm.

Corollary discharge inhibition and audition in the stridulating cricket.

The romantic notion of crickets singing on a warm summer's evening is quickly dispelled when one comes ear to ear with a stridulating male. Remarkably, stridulating male crickets are able to hear sounds from the environment despite generating a 100 db song (Heiligenberg 1969; Jones and Dambach 1973). This review summarises recent work examining how they achieve this feat of sensory processing. While the responsiveness of the crickets' peripheral auditory system (tympanic membrane, tympanic nerve, state of the acoustic spiracle) is maintained during sound production, central auditory neurons are inhibited by a feedforward corollary discharge signal precisely timed to coincide with the auditory neurons' maximum response to self-generated sound. In this way, the corollary discharge inhibition prevents desensitisation of the crickets' auditory pathway during sound production.

Mechanisms underlying phonotactic steering in the cricket Gryllus bimaculatus revealed with a fast trackball system.

Phonotactic steering behaviour of the cricket G. bimaculatus was analysed with a new highly sensitive trackball system providing a spatial and temporal resolution of 127 microm and 0.3 ms, respectively. Orientation to artificial calling songs started at 45 dB SPL, it increased up to 75 dB SPL and then saturated. When exposed to two identical patterns of different intensity, crickets significantly steered towards the louder sound pattern, whenever the intensity difference was greater than 1 dB. Bilateral latency differences in sound presentation did not always cause clear orientation towards the leading side. The overall walking direction depended on the number of sound pulses perceived from the left or right side with the animals turning towards the side providing the larger number of pulses. The recordings demonstrated rapid changes in walking direction performed even during a chirp. These rapid steering responses occurred with a latency of 55-60 ms, well before the central nervous system had time to evaluate the temporal structure of a whole chirp. When every other sound pulse was presented from opposite directions, the crickets followed the temporal pattern of sound presentation and rapidly steered towards the left and right side. Steering towards individual sound pulses does not agree with the proposal that crickets analyse the quality of sound patterns and then steer towards the better pattern. Rather, these experiments suggest that fast steering to single sound pulses determines the lateral deviation of the animals and that complex auditory orientation emerges from this simple mechanism of auditory steering.

Temporal pattern recognition based on instantaneous spike rate coding in a simple auditory system.

Auditory pattern recognition by the CNS is a fundamental process in acoustic communication. Because crickets communicate with stereotyped patterns of constant frequency syllables, they are established models to investigate the neuronal mechanisms of auditory pattern recognition. Here we provide evidence that for the neural processing of amplitude-modulated sounds, the instantaneous spike rate rather than the time-averaged neural activity is the appropriate coding principle by comparing both coding parameters in a thoracic interneuron (Omega neuron ON1) of the cricket (Gryllus bimaculatus) auditory system. When stimulated with different temporal sound patterns, the analysis of the instantaneous spike rate demonstrates that the neuron acts as a low-pass filter for syllable patterns. The instantaneous spike rate is low at high syllable rates, but prominent peaks in the instantaneous spike rate are generated as the syllable rate resembles that of the species-specific pattern. The occurrence and repetition rate of these peaks in the neuronal discharge are sufficient to explain temporal filtering in the cricket auditory pathway as they closely match the tuning of phonotactic behavior to different sound patterns. Thus temporal filtering or "pattern recognition" occurs at an early stage in the auditory pathway.

A corollary discharge mechanism modulates central auditory processing in singing crickets.

Crickets communicate using loud (100 dB SPL) sound signals that could adversely affect their own auditory system. To examine how they cope with this self-generated acoustic stimulation, intracellular recordings were made from auditory afferent neurons and an identified auditory interneuron-the Omega 1 neuron (ON1)-during pharmacologically elicited singing (stridulation). During sonorous stridulation, the auditory afferents and ON1 responded with bursts of spikes to the crickets' own song. When the crickets were stridulating silently, after one wing had been removed, only a few spikes were recorded in the afferents and ON1. Primary afferent depolarizations (PADs) occurred in the terminals of the auditory afferents, and inhibitory postsynaptic potentials (IPSPs) were apparent in ON1. The PADs and IPSPs were composed of many summed, small-amplitude potentials that occurred at a rate of about 230 Hz. The PADs and the IPSPs started during the closing wing movement and peaked in amplitude during the subsequent opening wing movement. As a consequence, during silent stridulation, ON1's response to acoustic stimuli was maximally inhibited during wing opening. Inhibition coincides with the time when ON1 would otherwise be most strongly excited by self-generated sounds in a sonorously stridulating cricket. The PADs and the IPSPs persisted in fictively stridulating crickets whose ventral nerve cord had been isolated from muscles and sense organs. This strongly suggests that the inhibition of the auditory pathway is the result of a corollary discharge from the stridulation motor network. The central inhibition was mimicked by hyperpolarizing current injection into ON1 while it was responding to a 100 dB SPL sound pulse. This suppressed its spiking response to the acoustic stimulus and maintained its response to subsequent, quieter stimuli. The corollary discharge therefore prevents auditory desensitization in stridulating crickets and allows the animals to respond to external acoustic signals during the production of calling song.