Heterogeneity of intrinsic biophysical properties among cochlear nucleus neurons improves the population coding of temporal information.

Reliable representation of the spectrotemporal features of an acoustic stimulus is critical for sound recognition. However, if all neurons respond with identical firing to the same stimulus, redundancy in the activity patterns would reduce the information capacity of the population. We thus investigated spike reliability and temporal fluctuation coding in an ensemble of neurons recorded in vitro from the avian auditory brain stem. Sequential patch-clamp recordings were made from neurons of the cochlear nucleus angularis while injecting identical filtered Gaussian white noise currents, simulating synaptic drive. The spiking activity in neurons receiving these identically fluctuating stimuli was highly correlated, measured pairwise across neurons and as a pseudo-population. Two distinct uncorrelated noise stimuli could be discriminated using the temporal patterning, but not firing rate, of the spike trains in the neural ensemble, with best discrimination using information at time scales of 5-20 ms. Despite high cross-correlation values, the spike patterns observed in individual neurons were idiosyncratic, with notable heterogeneity across neurons. To investigate how temporal information is being encoded, we used optimal linear reconstruction to produce an estimate of the original current stimulus from the spike trains. Ensembles of trains sampled across the neural population could be used to predict >50% of the stimulus variation using optimal linear decoding, compared with ∼20% using the same number of spike trains recorded from single neurons. We conclude that heterogeneity in the intrinsic biophysical properties of cochlear nucleus neurons reduces firing pattern redundancy while enhancing representation of temporal information.