A Sensitive Period for the Impact of Hearing Loss on Auditory Perception

Buran, Bradley N.; Sarro, Emma C.; Manno, Francis A. M.; Kang, Ramanjot; Caras, Melissa L.; Sanes, Dan H.

doi:10.1523/jneurosci.0647-13.2014

Cited by 50 publications

(62 citation statements)

References 79 publications

(22 reference statements)

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“…This result is in line with an abundance of work demonstrating behaviorally gated modulations of ACx activity (37,(44)(45)(46)(47)(48)(49)(62)(63)(64)(65)(66). Our observation that disengaged neural sensitivity is better if measured immediately after behavioral testing, rather than before (compare green lines in Fig.…”

Section: Significancesupporting

confidence: 88%

Top-down modulation of sensory cortex gates perceptual learning

Caras

Sanes

2017

Proc. Natl. Acad. Sci. U.S.A.

100

108

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Practice sharpens our perceptual judgments, a process known as perceptual learning. Although several brain regions and neural mechanisms have been proposed to support perceptual learning, formal tests of causality are lacking. Furthermore, the temporal relationship between neural and behavioral plasticity remains uncertain. To address these issues, we recorded the activity of auditory cortical neurons as gerbils trained on a sound detection task. Training led to improvements in cortical and behavioral sensitivity that were closely matched in terms of magnitude and time course. Surprisingly, the degree of neural improvement was behaviorally gated. During task performance, cortical improvements were large and predicted behavioral outcomes. In contrast, during nontask listening sessions, cortical improvements were weak and uncorrelated with perceptual performance. Targeted reduction of auditory cortical activity during training diminished perceptual learning while leaving psychometric performance largely unaffected. Collectively, our findings suggest that training facilitates perceptual learning by strengthening both bottom-up sensory encoding and top-down modulation of auditory cortex.broad range of sensory skills improve with practice during perceptual learning (PL), including language acquisition (1-3), musical abilities (4), and recognition of emotions (5). The neural bases for such perceptual improvement may vary widely. For example, training-based changes in neural activity have been identified in a number of brain regions, including early (6-13) and late (14, 15) sensory cortices, multisensory regions (16, 17), and downstream decision-making areas (18). Similarly, several neural mechanisms have been proposed, such as enhanced signal representation (19), reduction of external (20, 21) or internal (22, 23) noise, and improvement in sensory readout or decision making (13,18,24,25).The apparent divergence of loci and mechanisms associated with PL could be due, in part, to limitations of experimental design. For example, some neural changes associated with PL are transient (26-29), making it necessary to monitor neural activity throughout the duration of perceptual training, rather than making comparisons only after PL is complete (6-12, 14-16, 30). For similar reasons, it is critical to block the function of a specific candidate brain region during training to determine whether it plays a causal role in PL. Although some reports show that manipulating brain activity can influence PL (28,(31)(32)(33)(34), there are no loss-of-function experiments to determine whether a particular region is required for behavioral improvement.To address these unresolved issues, we recorded from auditory cortex (ACx) as animals improved on an auditory detection task and, in separate experiments, blocked ACx activity during the period of perceptual training. We found that neural and behavioral sensitivity improved in a nearly identical manner over the course of training, in terms of both absolute magnitude and kinetics. Furthermore,...

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Section: Significancesupporting

confidence: 88%

Top-down modulation of sensory cortex gates perceptual learning

Caras

Sanes

2017

Proc. Natl. Acad. Sci. U.S.A.

100

108

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“…Even after treatment with hearing aids or cochlear implants, these individuals present with substantial deficits when attempting to extract target speech signals from background talkers. There are several potential factors that contribute to this difficultly, some of which are associated with peripheral pathology [e.g., reduced spectral resolution of auditory filters (78)], and others with impaired central processing (79)(80)(81). As the need to quickly and reliably extract signals from background noise is ubiquitous in work, educational, and social contexts, improved signal in noise extraction in these listening environments may improve quality of life for these individuals.…”

Section: Discussionmentioning

confidence: 99%

Immersive audiomotor game play enhances neural and perceptual salience of weak signals in noise

Whitton

Hancock

Polley

2014

Proc. Natl. Acad. Sci. U.S.A.

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All sensory systems face the fundamental challenge of encoding weak signals in noisy backgrounds. Although discrimination abilities can improve with practice, these benefits rarely generalize to untrained stimulus dimensions. Inspired by recent findings that action video game training can impart a broader spectrum of benefits than traditional perceptual learning paradigms, we trained adult humans and mice in an immersive audio game that challenged them to forage for hidden auditory targets in a 2D soundscape. Both species learned to modulate their angular search vectors and target approach velocities based on real-time changes in the level of a weak tone embedded in broadband noise. In humans, mastery of this tone in noise task generalized to an improved ability to comprehend spoken sentences in speech babble noise. Neural plasticity in the auditory cortex of trained mice supported improved decoding of low-intensity sounds at the training frequency and an enhanced resistance to interference from background masking noise. These findings highlight the potential to improve the neural and perceptual salience of degraded sensory stimuli through immersive computerized games.foraging | hearing | cortical | gradient search | noise suppression E fficient search for resources is critical to the survival of most species. As such, foraging represents a conserved, adaptive behavior that drives decision making under the types of naturalistic contexts for which brains have evolved. Efficient foraging involves the dynamic integration of sensory cues, memory, and the costs and values associated with foraging decisions (1-3). The sensory cues used to guide foraging can be either discrete or gradient-based. For instance, moths, dogs, and humans navigate odor gradients using characteristic casting and zigzagging behaviors in response to dynamic somatosensory and olfactory cues (4-6). Although the successful execution of these behaviors would be expected to strongly rely on the integration of rapidly changing, weak and noisy sensory information, previous work has primarily focused on computations involved in cost/value decisions related to the exploration/exploitation trade-off (1, 2, 7-9), rather than whether and how foraging behavior is refined through learned associations between these dynamic sensory cues and reinforcement signals (but see refs. 10-12).Accumulating evidence suggests that sensory learning in mature animals reflects the coordinated activation of sensory brain areas and neuromodulatory control nuclei (13). Of these neuromodulatory systems, cholinergic and dopaminergic neurons in the nucleus basalis and ventral tegmental area, respectively, have been observed to code cognitive operations of cue detection (14, 15) and reward prediction (16) associated with behaviorally relevant sensory stimuli and to subserve learning in complex sensory-guided tasks (17). Theoretically, these learning systems are maximally engaged by tasks that require the continuous interplay of sensory cues, dynamically updated motor action program...

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“…A surgical level of anesthesia was induced (methoxyflurane, Medical Developments International), and the malleus was removed through a perforation in the tympanic membrane. After recovery, animals were reared to adulthood with a permanent bilateral conductive loss of approximately 40 dB (Buran et al, 2014a; Rosen et al, 2012; Tucci et al, 1999). Normal hearing (NH) animals did not undergo a sham surgery.…”

Section: Experimental Approachesmentioning

confidence: 99%

“…Using an appetitive reinforcement operant conditioning procedure (Buran et al, 2014a), adult CHL and control animals were trained on an AM rate discrimination task. AM is a favorable acoustic feature to examine because it is an important component of most vocalizations, including speech (Elliott et al, 2009; Rosen, 1992; Singh et al, 2003).…”

Section: Introductionmentioning

confidence: 99%

Developmental hearing loss impedes auditory task learning and performance in gerbils

et al. 2017

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The consequences of developmental hearing loss have been reported to include both sensory and cognitive deficits. To investigate these issues in a non-human model, auditory learning and asymptotic psychometric performance were compared between normal hearing (NH) adult gerbils and those reared with conductive hearing loss (CHL). At postnatal day 10, before ear canal opening, gerbil pups underwent bilateral malleus removal to induce a permanent CHL. Both CHL and control animals were trained to approach a water spout upon presentation of a target (Go stimuli), and withhold for foils (Nogo stimuli). To assess the rate of task acquisition and asymptotic performance, animals were tested on an amplitude modulation (AM) rate discrimination task. Behavioral performance was calculated using a signal detection theory framework. Animals reared with developmental CHL displayed a slower rate of task acquisition for AM discrimination task. Slower acquisition was explained by an impaired ability to generalize to newly introduced stimuli, as compared to controls. Measurement of discrimination thresholds across consecutive testing blocks revealed that CHL animals required a greater number of testing sessions to reach asymptotic threshold values, as compared to controls. However, with sufficient training, CHL animals approached control performance. These results indicate that a sensory impediment can delay auditory learning, and increase the risk of poor performance on a temporal task.

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A Sensitive Period for the Impact of Hearing Loss on Auditory Perception

Cited by 50 publications

References 79 publications

Top-down modulation of sensory cortex gates perceptual learning

Top-down modulation of sensory cortex gates perceptual learning

Immersive audiomotor game play enhances neural and perceptual salience of weak signals in noise

Developmental hearing loss impedes auditory task learning and performance in gerbils

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