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.

Selective blockade of rat brain T-type calcium channels provides insights on neurophysiological basis of arousal dependent resting state functional magnetic resonance imaging signals

“…Anatomical and functional connections between rat barrel cortex and these brain areas have been observed in a number of studies ( Frostig et al, 2008 ; Bedwell et al, 2014 ; Zakiewicz et al, 2014 ). Right auditory cortex exhibited significantly increased FC to contralateral auditory, visual, and somatosensory areas, consistent with prior functional and anatomic tracing studies ( Smith et al, 2010 ; Schormans et al, 2016 ; Thomas et al, 2020 ). Thus, the suppression of arousal-dependent fMRI signals (QPPs) by TTA-P2 increases apparent intrinsic FC in cortical brain function networks as hypothesized.…”

Temporal Alterations to Central Auditory Processing without Synaptopathy after Lifetime Exposure to Environmental Noise

“…We investigated whether a similar robustness applied at the cortical level. The adult brain is much more resistant to experiencedependent plasticity than the juvenile brain (Keuroghlian and Knudsen 2007), but several studies have shown that prolonged exposures at non-traumatic levels can trigger massive, albeit reversible, plastic changes at the cortical level (Noreña et al 2006;Pienkowski et al 2011;Zheng 2012;Zhou and Merzenich 2012;Lau et al 2015;Thomas, Guercio, et al 2019;Thomas et al 2020). Unlike Zheng (2012), we found no signs of tonotopy disruption in our animals, whatever the duration of exposure (Supp.…”

“…This reorganization may be governed by homeostatic plasticity (Gourévitch et al 2014) and is partially reversible over a few weeks (Pienkowski and Eggermont 2012). Long-term noise exposure may also favor subsequent plastic changes, as if a new critical window had been opened in adulthood (Zhou et al 2011;Thomas, Friedman, et al 2019;Thomas et al 2020), but could also lead to auditory disorders, such as hyperacusis (Thomas, Guercio, et al 2019).…”

Visuomotor association orthogonalizes visual cortical population codes

“…Finally, expansion of sites responding to task stimuli is a transient phenomenon. After continued training or stimulus exposure, expanded maps can “renormalize” to their original state without compromising behavioral performance 45 ; furthermore, induction of map expansion by means other than task training can actually worsen task performance 46 , in particular by increasing the rate of false responses to non-target stimuli 47 . Our task required a long training period, potentially allowing time for map expansion to reverse; it also requires differentially responding to the two stimuli while not responding to the similar distractor stimulus, for which map expansion might actually impair performance.…”