Encoding of small-scale air motion dynamics in the cricket, Acheta domesticus.

The cercal sensory system of cricket mediates the detection, localization, and identification of air current signals generated by predators, mates, and competitors. This mechanosensory system has been used extensively for experimental and theoretical studies of sensory coding at the cellular and system levels. It is currently thought that sensory interneurons (INs) in the terminal abdominal ganglion extract information about the direction, velocity, and acceleration of the air currents in the animal's immediate environment and project a coarse-coded representation of those parameters to higher centers. All feature detection is thought to be carried out in higher ganglia by more complex, specialized circuits. We present results that force a substantial revision of current hypotheses. Using multiple extracellular recordings and a special sensory stimulation device, we demonstrate that four well-studied interneurons in this system respond with high sensitivity and selectivity to complex dynamic multidirectional features of air currents that have a spatial scale smaller than the physical dimensions of the cerci. The INs showed much greater sensitivity for these features than for unidirectional bulk-flow stimuli used in previous studies. Thus, in addition to participating in the ensemble encoding of bulk airflow stimulus characteristics, these interneurons are capable of operating as feature detectors for naturalistic stimuli. In this sense, these interneurons are encoding and transmitting information about different aspects of their stimulus environment; they are multiplexing information. Major aspects of the stimulus-response specificity of these interneurons can be understood from the dendritic anatomy and connectivity with the sensory afferent map.NEW & NOTEWORTHY A set of sensory interneurons that have been studied for over 30 years by several different research groups were discovered to have previously unknown encoding characteristics. As well as encoding the direction of bulk airflow with a coarse-coding scheme as shown in previous studies, these interneurons are also responsive to very small-scale, directionally complex air current waveforms. This feature sensitivity can be understood in terms of the cells' complex dendritic branching patterns.

The cricket cercal system implements delay-line processing.

The cercal sensory system of crickets mediates sensitivity to low-amplitude air currents. The sense organ for this system is a pair of antenna-like abdominal appendages called cerci, each of which is about 1 cm long in normal adult crickets. Although this system has been used extensively as a model system for studying the mechanisms underlying neural coding at the cellular and system levels, no previous studies have considered the functional significance of the physical dimensions of cerci. We show that the differential conduction characteristics of the receptor array in Acheta domesticus crickets are of substantial significance. All filiform sensory afferent axons we examined had the same propagation speeds to within a small variance, resulting in a significant and systematic differential propagation time for spikes from sensory receptors at different locations along the structure. Thus the sensory structures operate as delay lines. The delay-line structure supports neural computations in many of the projecting cercal interneurons (INs) that yield substantial differential sensitivity to the direction and velocity of naturalistic stimuli. Several INs show delay-line-derived sensitivities that are equivalent, in an engineering sense, to "notch filtering," through which background noise is selectively eliminated by the delay-line-based processing.

Distinct gamma2 subunit domains mediate clustering and synaptic function of postsynaptic GABAA receptors and gephyrin.

Modulation of the concentration of postsynaptic GABA(A) receptors contributes to functional plasticity of inhibitory synapses. The gamma2 subunit of GABA(A) receptor is specifically required for clustering of these receptors, for recruitment of the submembrane scaffold protein gephyrin to postsynaptic sites, and for postsynaptic function of GABAergic inhibitory synapses. To elucidate this mechanism, we here have mapped the gamma2 subunit domains required for restoration of postsynaptic clustering and function of GABA(A) receptors in gamma2 subunit mutant neurons. Transfection of gamma2-/- neurons with the gamma2 subunit but not the alpha2 subunit rescues postsynaptic clustering of GABA(A) receptors, results in recruitment of gephyrin to postsynaptic sites, and restores the amplitude and frequency of miniature inhibitory postsynaptic currents to wild-type levels. Analogous analyses of chimeric gamma2/alpha2 subunit constructs indicate, unexpectedly, that the fourth transmembrane domain of the gamma2 subunit is required and sufficient for postsynaptic clustering of GABA(A) receptors, whereas cytoplasmic gamma2 subunit domains are dispensable. In contrast, both the major cytoplasmic loop and the fourth transmembrane domain of the gamma2 subunit contribute to efficient recruitment of gephyrin to postsynaptic receptor clusters and are essential for restoration of miniature IPSCs. Our study points to a novel mechanism involved in targeting of GABA(A) receptors and gephyrin to inhibitory synapses.