Rapid and long-lasting improvements in neural discrimination of acoustic signals with passive familiarization

Sensory representations in the adult brain must undergo dynamic changes to adapt to the complexity of the external world. This study investigated how passive exposure to novel sounds modifies neural representations to facilitate recognition and discrimination, using the zebra finch model organism. The neural responses in an auditory structure in the zebra finch brain, Caudal Medial Nidopallium (NCM), undergo a long-term form of adaptation with repeated stimulus presentation, providing an excellent substrate to probe the neural underpinnings of adaptive sensory representations. In Experiment 1, electrophysiological activity in NCM was recorded under passive listening conditions as novel natural vocalizations were familiarized through playback. Neural decoding of stimuli using the temporal profiles of both single-unit and multi-unit responses improved dramatically during the first few stimulus presentations. During subsequent encounters, these signals were recognized after hearing fewer initial acoustic features. Remarkably, the accuracy of neural decoding was higher when different stimuli were heard in separate blocks compared to when they were presented randomly in a shuffled sequence. NCM neurons with narrow spike waveforms generally yielded higher neural decoding accuracy than wide spike neurons, but the rate at which these accuracies improved with passive exposure was comparable between the two neuron types. Experiment 2 supported and extended these findings by showing that the rapid gains in neural decoding of novel vocalizations with passive familiarization were long-lasting, maintained for 20 hours after the initial encounter, in multi-unit responses. Taken together, these findings provide valuable insights into the mechanisms by which the nervous system dynamically modulates sensory representations to improve discrimination of novel complex signals over short and long timescales. Similar mechanisms may also be engaged during processing of human speech signals, and thus may have potential translational relevance for elucidating the neural basis of speech comprehension difficulties.