Developmental hearing loss impedes auditory task learning and performance in gerbils

Abstract

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.

Preserving Inhibition during Developmental Hearing Loss Rescues Auditory Learning and Perception

“…Adults reared with permanent conductive HL display poorer performance on frequency modulation detection, AM detection, AM discrimination, and modulation masking release tasks (Rosen et al, 2012;Buran et al, 2014;Ihlefeld et al, 2016;von Trapp et al, 2017;Yao and Sanes, 2018). Furthermore, adult animals reared with conductive HL display slower task learning and perceptual learning (von Trapp et al, 2017). Similar results were found for juvenile animals following a brief period of HL that occurs during a well-defined critical period (Caras and Sanes, 2015;Mowery et al, 2015Mowery et al, , 2016.…”

“…We have found that developmental HL impairs several auditory perceptual skills, as well as task learning. Adults reared with permanent conductive HL display poorer performance on frequency modulation detection, AM detection, AM discrimination, and modulation masking release tasks (Rosen et al, 2012;Buran et al, 2014;Ihlefeld et al, 2016;von Trapp et al, 2017;Yao and Sanes, 2018). Furthermore, adult animals reared with conductive HL display slower task learning and perceptual learning (von Trapp et al, 2017).…”

The Sensory Striatum Is Permanently Impaired by Transient Developmental Deprivation

“…Thus, early dysfunctional connectivity between the cortex and the striatum could lead to the gradual emergence of striatal related symptoms for ADHD (Braz et al, 2015), autism (Peixoto et al, 2016), schizophrenia (Morris et al, 2015), Parkinson's Disease (Stephens et al, 2005), Huntington's Disease (Cepeda et al, 2007), and Tourette's Syndrome (Israelashvili and Bar-Gad, 2015). Likewise, a compromised corticostriatal pathway may contribute to some non-sensory deficits that accompany developmental HL (Reichman and Healey 1983; Teele et al 1990; Schönweiler et al 1998; Pisoni et al 2011; Beer et al 2014; Kronenberger et al 2014; Caras and Sanes, 2015; von Trapp et al, 2016). Our results provide one mechanism by which early changes to striatal cellular physiology during a critical period could lead to long-term cognitive impairments in a broad range of neurological and sensory disorders.…”

“…Developmental HL imposes a risk for deficiencies in cognitive skills (Adesman et al, 1990; Burkholder-Juhasz et al, 2007; Watson et al, 2007; Pisoni et al, 2011; Beer et al, 2014; Kronenberger et al, 2014; von Trapp et al, 2016). Even a transient period of developmental HL diminishes perceptual skills long after the deprivation has ended (Hall et al, 1995; Caras and Sanes, 2015).…”

Impaired sensitivity to temporal fine structure but not the envelope for children with mild-to-moderate sensorineural hearing loss

“…Moreover, studies involving adults with predominantly acquired losses (i.e., presbycusis) are not designed to assess the developmental effects of SNHL during childhood. Recent findings from animal studies suggest that even moderate levels of conductive hearing loss during critical periods may have a substantial, negative impact upon auditory perceptual development (Buran et al, 2014;Caras and Sanes, 2015;Rosen et al, 2012;von Trapp et al, 2017). We might therefore expect a greater, or altered effect of MMHL during childhood on the development of a variety of measures of AP.…”