Perceptual Learning Directs Auditory Cortical Map Reorganization through Top-Down Influences

Abstract

The primary sensory cortex is positioned at a confluence of bottom-up dedicated sensory inputs and top-down inputs related to higherorder sensory features, attentional state, and behavioral reinforcement. We tested whether topographic map plasticity in the adult primary auditory cortex and a secondary auditory area, the suprarhinal auditory field, was controlled by the statistics of bottom-up sensory inputs or by top-down task-dependent influences. Rats were trained to attend to independent parameters, either frequency or intensity, within an identical set of auditory stimuli, allowing us to vary task demands while holding the bottom-up sensory inputs constant. We observed a clear double-dissociation in map plasticity in both cortical fields. Rats trained to attend to frequency cues exhibited an expanded representation of the target frequency range within the tonotopic map but no change in sound intensity encoding compared with controls. Rats trained to attend to intensity cues expressed an increased proportion of nonmonotonic intensity response profiles preferentially tuned to the target intensity range but no change in tonotopic map organization relative to controls. The degree of topographic map plasticity within the task-relevant stimulus dimension was correlated with the degree of perceptual learning for rats in both tasks. These data suggest that enduring receptive field plasticity in the adult auditory cortex may be shaped by task-specific top-down inputs that interact with bottom-up sensory inputs and reinforcement-based neuromodulator release. Top-down inputs might confer the selectivity necessary to modify a single feature representation without affecting other spatially organized feature representations embedded within the same neural circuitry.

Spectral integration plasticity in cat auditory cortex induced by perceptual training

“…The literature is currently divided between studies demonstrating that receptive field plasticity in AI is dictated by stimulus input statistics under conditions of varying (Polley et al, 2004) or absent (Kilgard et al, 2001) task demands and studies that demonstrate that AI receptive field plasticity is relatively independent of stimulus statistics, but instead is guided by the demands of the conditioning task (Polley et al, 2006). The present results most strongly support findings that receptive field reorganization is directed by statistics of sensory inputs paired with behavioral reinforcement.…”

“…Discrimination thresholds for shifts in the spectral envelope improved steadily over the course of the behavioral training, similar to other auditory discrimination tasks (e.g., Prosen et al;Recanzone et al, 1993;Polley et al, 2006). Analysis of the hit rate and false-alarm rate early and late in training support the conclusion that the observed improvements in discrimination reflect changes in perceptual capacity and not changes in response criterion.…”

“…In conditioning tasks in which the irrelevant sensory inputs need not be suppressed to accurately perform the task, receptive field reorganization might be directed by the bottom-up statistics of sensory stimuli that are: i) paired with reinforcement and ii) substantially different from the naïve animal's ambient acoustic environment. In conditioning tasks where irrelevant stimulus features compete for limited attentional resources or are otherwise antithetical to accurate task performance, their influence might be suppressed through top-down influences (see, for example, Ahissar et al, 1993;Li et al, 2004;Polley et al, 2006).…”

“…It was found that animals discriminate many speech-like features in a similar fashion as humans. The ability to discriminate signals can improve with training and is accompanied by plastic changes in response characteristics of central auditory neurons (e.g., Allard et al, 1992;Bakin et al, 1996;Beitel et al, 2001;Edeline, 1999;Recanzone et al, 1993;Polley et al 2004Polley et al , 2006Prosen et al, 1990;Weinberger et al, 1988). Since the process of behavioral assessment can influence the perceptual capacity of an animal, it may not be valid to equate physiological data from untrained animals with the psychophysical performance of trained animal.…”

Plasticity of human auditory-evoked fields induced by shock conditioning and contingency reversal

“…Auditory plasticity can reflect stimulus features as well as top-down, task-related factors (e.g., ref. 7).…”