Modifying the Adult Rat Tonotopic Map with Sound Exposure Produces Frequency Discrimination Deficits That Are Recovered with Training.

ABSTRACT

Frequency discrimination learning is often accompanied by an expansion of the functional region corresponding to the target frequency within the auditory cortex. Although the perceptual significance of this plastic functional reorganization remains debated, greater cortical representation is generally thought to improve perception for a stimulus. Recently, the ability to expand functional representations through passive sound experience has been demonstrated in adult rats, suggesting that it may be possible to design passive sound exposures to enhance specific perceptual abilities in adulthood. To test this hypothesis, we exposed adult female Long-Evans rats to 2 weeks of moderate-intensity broadband white noise followed by 1 week of 7 kHz tone pips, a paradigm that results in the functional over-representation of 7 kHz within the adult tonotopic map. We then tested the ability of exposed rats to identify 7 kHz among distractor tones on an adaptive tone discrimination task. Contrary to our expectations, we found that map expansion impaired frequency discrimination and delayed perceptual learning. Rats exposed to noise followed by 15 kHz tone pips were not impaired at the same task. Exposed rats also exhibited changes in auditory cortical responses consistent with reduced discriminability of the exposure tone. Encouragingly, these deficits were completely recovered with training. Our results provide strong evidence that map expansion alone does not imply improved perception. Rather, plastic changes in frequency representation induced by bottom-up processes can worsen perceptual faculties, but because of the very nature of plasticity these changes are inherently reversible.SIGNIFICANCE STATEMENT The potent ability of our acoustic environment to shape cortical sensory representations throughout life has led to a growing interest in harnessing both passive sound experience and operant perceptual learning to enhance mature cortical function. We use sound exposure to induce targeted expansions in the adult rat tonotopic map and find that these bottom-up changes unexpectedly impair performance on an adaptive tone discrimination task. Encouragingly, however, we also show that training promotes the recovery of electrophysiological measures of reduced neural discriminability following sound exposure. These results provide support for future neuroplasticity-based treatments that take into account both the sensory statistics of our external environment and perceptual training strategies to improve learning and memory in the adult auditory system.