Temporal integration vs. parallel processing: coping with the variability of neuronal messages in directional hearing of insects

The behaviour of many animals indicates a high precision in the processing of sensory signals, which often seems at odds with the large variability of individual neuronal responses. Using the directional hearing of the grassh opper Chorthippus biguttulus (Ch. biguttulus) as a model system, we investi gated the possible contributions of temporal integration and parallel proce ssing at the receptor level to the observed behavioural acuity. The precisi on of the animals' phonotactic orientation behaviour to stimuli of differen t durations was measured and compared with the spiking responses of auditor y receptor cells, leading to the following results. A behavioural decision based on integrating the spikes from a pair of receptors (one cell in each ear) over a 1000-ms time window would substantially decrease the error prob ability, compared with evaluating a 250-ms period. The animal as a whole, h owever, responded as precisely to a 250 ms stimulus as to a stimulus of nat ural duration (c. 1000 ms). A phonotactic decision based on a 1.5 dB intens ity difference between the ears corresponds to a spike count difference of approximately 1 spike per 100 ms in a pair of receptors. As these differenc es are in the order of the statistical spike count fluctuations, the error probabilities for an ideal observer of the spike count are substantially hi gher (13-18%) than the errors observed in the behavioural tests (only 5%). We conclude that the animals' nervous system has to sample information from a pool of 6-13 receptors to arrive at the observed behavioural precision.