The emphasis of deafness research has been to establish the long-term consequences of permanent hearing loss. However, auditory processing deficits can be induced by transient hearing loss during childhood. These deficits in perception, speech, and language processing can persist long after normal audibility is restored. One explanation for the persistence of these deficits is that transient hearing loss causes irreversibl changes to CNS cellular properties that may lead to degraded stimulus encoding. Therefore, this proposal will evaluate the premise that transient, mild hearing loss during development induces behavioral deficits that are associated with sensory and non-sensory neural deficits. Auditory cortex responses from multiple sites will be recorded telemetrically from gerbils with a history of transient hearing loss as they train on, and perform, auditory psychophysical tasks. The core hypothesis: Perceptual deficits that accompany transient developmental hearing loss are attributable both to degraded sensory processing (e.g., encoding of acoustic parameters) and non-sensory mechanisms (e.g., increased neural response during task performance).
Three aims test predictions emerging from this hypothesis:
Aim 1 will determine whether there is a specific developmental epoch during which perceptual skills are vulnerable to transient hearing loss; animals will be reared with bilateral earplugs beginning during one of three age ranges. In all cases, psychometric performance will be assessed on two auditory tasks, amplitude (AM) or frequency modulation (FM) depth detection. Normal cochlear function will be confirmed with ABR measurements following earplug removal.
Aim 2 : To determine whether perceptual deficits induced by transient hearing loss are associated with a degraded sensory representation, an electrode array will be implanted in the primary auditory cortex, and neural responses will be recorded telemetrically as each animal is trained and tested on one of the tasks described in Aim 1. Neurometric functions will be compared directly to psychometric functions obtained during the same trials, permitting us to establish whether sensory encoding is impaired by transient hearing loss, and whether the magnitude of impairment could explain the perceptual deficits of individual animals.
Aim 3 : To determine whether the perceptual deficits induced by transient hearing loss is correlated with disruption of a non-sensory mechanism, we will compare neural responses to identical acoustic parameters as a function of listening state: during task performance versus during passive listening (i.e., a period when animals are not engaged in a task). This experiment will permit us to establish whether a non-sensory mechanism is correlated with the magnitude of perceptual deficits within individual animals. Together, these Aims will reveal whether there is a developmental period during which transient hearing loss disrupts the maturation of sensory and non-sensory mechanisms that support perceptual performance. The implication is that persistent neural processing deficits may present an enduring barrier to learning or improving on novel auditory perceptual skills.

Public Health Relevance

Transient hearing loss in children can induce long-lasting deficits in auditory-based communication, and these behavioral problems have been attributed to central nervous system deficits. This proposal will evaluate the premise that a brief period of transient developmental hearing loss can induce perceptual deficits that are associated with specific auditory cortical processing deficits. The long-term implication is that central nervous system processing deficits can explain the barriers to auditory perception or learning that persist long after hearing thresholds return to normal.

Agency
National Institute of Health (NIH)
Institute
National Institute on Deafness and Other Communication Disorders (NIDCD)
Type
Research Project (R01)
Project #
5R01DC014656-05
Application #
9674442
Study Section
Auditory System Study Section (AUD)
Program Officer
Poremba, Amy
Project Start
2015-04-01
Project End
2021-03-31
Budget Start
2019-04-01
Budget End
2021-03-31
Support Year
5
Fiscal Year
2019
Total Cost
Indirect Cost
Name
New York University
Department
Neurosciences
Type
Schools of Arts and Sciences
DUNS #
041968306
City
New York
State
NY
Country
United States
Zip Code
10012
Yao, Justin D; Sanes, Dan H (2018) Developmental deprivation-induced perceptual and cortical processing deficits in awake-behaving animals. Elife 7:
von Trapp, Gardiner; Aloni, Ishita; Young, Stephen et al. (2017) Developmental hearing loss impedes auditory task learning and performance in gerbils. Hear Res 347:3-10
Caras, Melissa L; Sanes, Dan H (2017) Top-down modulation of sensory cortex gates perceptual learning. Proc Natl Acad Sci U S A 114:9972-9977
von Trapp, Gardiner; Buran, Bradley N; Sen, Kamal et al. (2016) A Decline in Response Variability Improves Neural Signal Detection during Auditory Task Performance. J Neurosci 36:11097-11106
Ihlefeld, Antje; Chen, Yi-Wen; Sanes, Dan H (2016) Developmental Conductive Hearing Loss Reduces Modulation Masking Release. Trends Hear 20:2331216516676255
Caras, Melissa L; Sanes, Dan H (2015) Sustained Perceptual Deficits from Transient Sensory Deprivation. J Neurosci 35:10831-42