Mild Hearing Loss Can Impair Brain Function The emphasis of hearing loss research has been to establish the long-term consequences of permanent, severe to profound deafness. However, auditory processing deficits can be induced by transient, mild hearing loss during childhood. These deficits in perception, speech, and language processing can persist long after normal audibility is restored. One ... Article
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Article  |   April 14, 2016
Mild Hearing Loss Can Impair Brain Function
Author Affiliations & Notes
  • Dan H. Sanes
    Center for Neural Science, New York University, New York, NY
  • Disclosures
    Disclosures ×
  • Financial: The author has no relevant financial interests to disclose.
    Financial: The author has no relevant financial interests to disclose.×
  • Nonfinancial: The author has previously published in the subject area.
    Nonfinancial: The author has previously published in the subject area.×
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Hearing Disorders / Part 1
Article   |   April 14, 2016
Mild Hearing Loss Can Impair Brain Function
Perspectives of the ASHA Special Interest Groups, April 2016, Vol. 1, 4-16. doi:10.1044/persp1.SIG6.4
History: Received January 31, 2016 , Revised February 25, 2016 , Accepted February 26, 2016
Perspectives of the ASHA Special Interest Groups, April 2016, Vol. 1, 4-16. doi:10.1044/persp1.SIG6.4
History: Received January 31, 2016; Revised February 25, 2016; Accepted February 26, 2016

The emphasis of hearing loss research has been to establish the long-term consequences of permanent, severe to profound deafness. However, auditory processing deficits can be induced by transient, mild 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 irreversible changes to the central nervous system (CNS) cellular properties that may lead to degraded stimulus encoding. Therefore, this review evaluates the premise that mild hearing loss during development induces behavioral deficits, and that these auditory deficits are causally related to changes within the CNS.

Deafness research emphasizes the consequences of permanent, profound hearing loss. There are three logical reasons for this priority. First, as the magnitude of hearing loss increases, the rate of diagnosis increases. Thus, newborn hearing screens typically identify those infants who have a loss greater than 30–40 dB HL (Johnson et al., 2005; Morton & Nance, 2006; Prieve et al., 2013); infants with mild hearing loss are treated as normal hearing and pass into the educational system without intervention. Second, the biological locus for profound hearing loss is usually the cochlea, offering both clinicians and basic research scientists an obvious therapeutic target. Clinicians gravitate towards peripheral prosthetic devices, while research scientists are hot in the pursuit of hair cell regeneration. Third, subjects with profound hearing loss, both human and nonhuman, display large behavioral effects, as compared to control populations. A large effect size (e.g., standardized difference between two means) can improve the clinician'elihood of discovering a treatment strategy that mitigates hearing difficulties, and the basic research scientist’s prospect of tracking down the biological explanation for a deficit. Therefore, it is unsurprising that mild hearing loss has been de-emphasized, both in research and treatment, making it a form of hearing loss that is often “unheeded.”
One might wonder why a basic research scientist would devote considerable resources to studying mild hearing loss, given the apparent lack of urgency. One intellectual reason for studying mild hearing loss in a nonhuman model emerges from a general theory of development—Sensory experience during finite periods of maturation, called critical periods (CPs), influences the central nervous system (CNS) function, thereby shaping adult perceptual skills. This heightened degree of plasticity is valuable because it enables the acquisition of complex skills, such as language or music. However, this plasticity comes with a cost; the CNS development displays an increased vulnerability to the sensory environment. Support for this theory is based on the neural and behavioral effects of sensory deprivation such as blindness and hearing loss (reviewed in Sanes, Harris, & Reh, 2012). An important axiom of this theory is that the deficits that attend developmental hearing loss can be minimized when hearing is restored before CPs close.
One practical reason for studying mild hearing loss arises from epidemiological estimates which suggest that the population of children with mild to moderate hearing loss is thought to be large (Niskar et al., 1998). A 2005 NIDCD Statistical Report on the “Prevalence of Hearing Loss in U.S. Children” estimated that upwards of 887,000 would be expected to have mild to moderate hearing loss, and ~3 million with a unilateral loss (National Institute on Deafness and Other Communication Disorders, 2010). In contrast, the estimate for severe to profound hearing loss was no more than 73,000, an order of magnitude lower. Therefore, if mild hearing loss does constitute a health concern, then it is risk faced by a large percentage of children.
One strategic reason for conducting research on the biological mechanisms that attend mild hearing loss is that this paradigm offers the best opportunity to identify CNS deficits that could explain impairments in auditory processing. Hearing research scientists who study the CNS seek to identify cellular properties that can account for auditory perceptual skills, or deficits in these skills. However, cochlear processing determines our perceptual performance across all three basic acoustic dimensions: frequency, sound level, and temporal cues (Oxenham & Bacon, 2003). When biological changes occur to both the cochlea and the CNS following hearing loss, their impact on perception is convoluted. In fact, decades of basic research show us that sensory deprivation during development induces structural and functional changes within the CNS (reviewed in Sanes et al., 2012). Therefore, permanent conductive or sensorineural hearing loss that begins during early childhood alters the CNS. Figure 1 illustrates this conundrum. On one hand, it is possible to explain nearly all perceptual deficits with a locus of damage that is cochlear in origin; on the other hand, we know that significant changes to CNS functional properties attend hearing loss (discussed below). In principle, these CNS deficits could explain many of the same perceptual deficits. Thus, if both cochlear and CNS dysfunction are present in an individual, how is it possible to determine whether a behavioral deficit is due to dysfunction of one or both loci? To attribute behavioral deficits to a CNS mechanism, we require an experimental paradigm in which the cochlea functions normally at the time of testing, thereby permitting us to assess CNS mechanisms. As I discuss below, one way to accomplish this is to study the consequence of mild, transient developmental hearing loss.
Figure 1.

The Perceptual Deficits That Attend Hearing Loss Can Be Attributable to Peripheral (PNS) or Central Nervous System (CNS) Dysfunction.

  The Perceptual Deficits That Attend Hearing Loss Can Be Attributable to Peripheral (PNS) or Central Nervous System (CNS) Dysfunction.
Figure 1.

The Perceptual Deficits That Attend Hearing Loss Can Be Attributable to Peripheral (PNS) or Central Nervous System (CNS) Dysfunction.

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The Clinical Motivation for Conducting Basic Research on Mild Hearing Loss
The clinical literature suggests that long-lasting auditory processing deficits can be induced by the kind of mild, transient hearing loss that is prevalent in childhood. Of greatest consequence for children is that developmental hearing loss, including mild loss, is a risk factor for poor acquisition of speech, language, and auditory-based information processing (Blair, Peterson, & Viehweg, 1985; Davis, Elfenbein, Schum, & Bentler, 1986; Moeller, Tomblin, Yoshinaga-Itano, Connor, & Jerger, 2007; Nicholas & Geers, 2006). Even fluctuating mild hearing loss, such as that found during bouts of otitis media with effusion (OME), produces deficits in performance that can outlast the period of elevated hearing thresholds. A set of prospective studies have documented the cumulative incidence of OME at 83% by 3 years of age, and reported a significant association between days spent with a middle ear effusion and lower scores on cognitive and language tests at 7 years (Teele, Klein, & Rosner, 1989; Teele, Klein, Chase, Menyuk, & Rosner, 1990). In general, the studies on mild to moderate hearing loss that confirm impaired hearing also demonstrate subsequent deficits in perception, speech, or language processing that can persist for months to years, long after normal audibility is restored (otitis media: Hall & Grose, 1994a; Hall, Grose, Dev, Drake, & Pillsbury, 1998; Hall, Grose, & Pillsbury, 1995a; Hogan, Meyer, & Moore, 1996; Hogan & Moore, 2003; Pillsbury, Grose, & Hall, 1991; otosclerosis: Hall & Grose, 1994b; Hall, Grose, & Mendoza, 1995b; atresia: Wilmington, Gray, & Jahrsdoerfer, 1994; mild to moderate sensorineural hearing loss [SNHL]: Halliday & Bishop, 2005; Halliday & Bishop, 2006; Rance, McKay, & Grayden, 2004; reviews: Casby, 2001; Roberts et al., 2004; Whitton & Polley, 2011). Furthermore, children identified with delayed speech or language demonstrate a correlation with hearing loss severity, such that more severe speech and language delays are associated with more severe hearing loss, including a significant effect of fluctuating conductive hearing loss (Psillas, Psifidis, Antoniadou-Hitoglou, & Kouloulas, 2006; Schönweiler, Ptok, & Radu, 1998).
Some studies have drawn an association between childhood hearing loss and delayed cognitive abilities (Bennett & Furukawa, 1984; Feagans, Sanyal, Henderson, Collier, & Appelbaum, 1987; Manders & Tyberghein, 1984; Mody, Schwartz, Gravel, & Ruben, 1999; Psarommatis et al., 2001; Reichman & Healey, 1983; Schlieper, Kisilevsky, Mattingly, & Yorke, 1985; Teele et al., 1990). This raises the possibility that speech and language deficits could be due either to a compromised sensory processing mechanism or to auditory-based learning and memory deficits following early hearing loss (Briscoe, Bishop, & Norby, 2001; Burkholder & Pisoni, 2003; Cowan et al., 1997; Davis et al., 1986; Gravel, Wallace, & Ruben, 1996; Kronenberger, Beer, Castellanos, Pisoni, & Miyamoto, 2014; Mody et al., 1999; Pisoni & Cleary, 2003). For example, normal hearing children performed better than those with hearing loss on a test of rapid nonsense word learning across an age range of 5–14 years (Pittman, Lewis, Hoover, & Stelmachowicz, 2005). Furthermore, there is evidence that slight to mild childhood hearing loss is associated with a decline in phonological short-term memory (Briscoe et al., 2001; Park & Lombardino, 2012; Wake et al., 2006). Therefore, basic research studies should consider whether both sensory and nonsensory mechanisms are vulnerable to developmental hearing loss.
Although transient hearing loss is known to have an impact on auditory processing, it is not yet clear whether this effect is restricted to a CP. The best evidence for auditory CPs comes from clinical research on profoundly deaf children who receive cochlear implants. Children implanted at <18 months display steeper rates of improvement on receptive and expressive language tests, as compared to those implanted after 36 months (Niparko et al., 2010). These language deficits persist at least 6 years after implantation for the late implanted children (Tobey et al., 2013). A similar outcome is observed for children with early identified mild to moderate hearing loss. This group displays a larger incidence of language impairments (Bess Dodd-Murphy, & Parker, 1998; Delage & Tuller, 2007; Gilbertson & Kamhi, 1995; Moeller et al., 2010; Norbury, Bishop, & Briscoe, 2001; Tomblin et al., 2015). Furthermore, as expected for a CP of vulnerability, there is a positive effect of early intervention (Fulcher, Purcell, Baker, & Munro, 2012; Tomblin et al., 2015; Walker et al., 2015). For example, those who receive amplification by 3 months, and audiovisual intervention by 6 months, attain age-appropriate language milestones, whereas a homogenous cohort identified >12 months do not perform as well (Fulcher et al., 2012). Therefore, the human hearing loss literature is consistent with the developmental CP concept.
Basic Research on Hearing Loss
Nonhuman studies of hearing loss have demonstrated a greater vulnerability during developmental CPs. However, most animal studies have examined neural encoding, rather than perception. Thus, both peripheral and central auditory function are vulnerable to auditory trauma or deprivation during developmental CPs (peripheral nervous system: Bock & Saunders, 1977; Henry, 1973; Kujawa & Liberman, 2006; Lenoir & Pujol, 1980; Saunders & Hirsch, 1976; Stanek, Bock, Goran, & Saunders, 1977; Saunders & Chen, 1982; central nervous system: Aizawa & Eggermont, 2006, 2007; DeBello, Feldman, & Knudsen, 2001; Fallon, Irvine, & Shepherd, 2008; E. Knudsen, Knudsen, & Esterly, 1984a; Mogdans & Knudsen, 1993, 1994; Popescu & Polley, 2010; Raggio & Schreiner, 2003; Razak, Richardson, & Fuzessery, 2008; Rosen, Sarro, Kelly, & Sanes, 2012; Salvi, Wang, & Ding, 2000; Snyder et al., 2000; Takahashi et al., 2006; Wang, Ding, & Salvi, 2002; Yu, Wadghiri, Sanes, & Turnbull, 2005). In fact, even a transient period of monaural hearing loss causes persistent encoding deficits in auditory cortex (Polley, Thompson, & Guo, 2013). These experimental findings are consistent with the clinical literature showing that permanent functional changes to the CNS arise when cochlear prostheses are implanted at later ages (Gilley, Sharma, & Dorman, 2008; Ponton & Eggermont, 2001; Sharma, Gilley, Dorman, & Baldwin, 2007). Even transient childhood hearing loss has been associated with neural deficits (Folsom, Weber, & Thompson, 1983). Young children with a history of OME display abnormal neural responses to speech syllable variants after hearing has returned to normal, suggesting that diminished speech discrimination can outlast the transient hearing loss (Haapala et al. 2014). Together, these findings suggest that temporary periods of mild to moderate hearing loss, when induced during a developmental CP, cause persistent deficits to central auditory function that may impair auditory perception despite the return of normal peripheral function.
Those basic research studies that have explored CPs for auditory perception have assessed the impact of unilateral hearing loss on sound localization and binaural encoding (Clements & Kelly, 1978; Keating, Dahmen, & King, 2013a; Keating & King, 2013b; Knudsen et al., 1984a, Knudsen, Esterly, & Knudsen, 1984b; Moore et al. 1999). However, since OME is commonly bilateral in humans (Engel, Anteunis, Volovics, Hendriks, & Marres, 1999), it is important to study binaural hearing loss. Furthermore, no animal studies have examined the impact of transient hearing loss (unilateral or bilateral) on the perception of spectral or temporal cues that support vocal communication.
Can CNS Deficits Explain Perceptual Impairments?
Our laboratory asks whether developmental hearing loss induces perceptual deficits that are attributable to impaired CNS mechanisms. We first studied an animal model of profound hearing loss (bilateral cochlea removal), and assessed CNS synapses in slices of brain tissue. Here, intracellular recordings can be obtained from individual auditory CNS neurons while electrically stimulating their synaptic connections. Figure 2 illustrates the basic experimental approach and one of the general findings. Following a period of SNHL, inhibitory synaptic responses are reduced in amplitude. This is observed in two regions of the auditory brainstem, the lateral superior olive and the inferior colliculus, and in the auditory cortex (Kotak & Sanes, 1996; Takesian, Kotak, & Sanes, 2010; Vale & Sanes, 2000). In fact, we have identified a broad range of synaptic deficits that emerge following SNHL, both at inhibitory and excitatory connections (Kotak et al., 2005; Kotak & Sanes, 1997; Kotak, Takesian, & Sanes, 2008; Vale, Juiz, Moore, & Sanes, 2004; Sarro, Kotak, Sanes, & Aoki, 2008; Takesian, Kotak, Sharma, & Sanes, 2013; Vale & Sanes, 2002; Vale, Schoorlemmer, & Sanes, 2003). Therefore, there is clear evidence that profound developmental hearing loss can induce dramatic changes in synapse function.
Figure 2.

Sensorineural Hearing Loss (SNHL) Causes a Decrease in the Strength of Inhibitory Synapses.

  Sensorineural Hearing Loss (SNHL) Causes a Decrease in the Strength of Inhibitory Synapses.
Figure 2.

Sensorineural Hearing Loss (SNHL) Causes a Decrease in the Strength of Inhibitory Synapses.

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To determine whether such changes would occur in response to less severe forms of hearing loss, we turned our attention to experimental models of conductive hearing loss (CHL). In the first model, the malleus bone was removed bilaterally in juvenile animals, resulting in a permanent moderate hearing loss of about 45 dB (Rosen et al., 2012; Xu, Kotak, & Sanes, 2007;). In the second model, we inserted earplugs bilaterally on postnatal day 11 at the time when ear canals open naturally. This results in a mild hearing loss of about 25 dB (Caras & Sanes, 2015; Mowery et al., 2015;). As illustrated in Figure 3, profound, moderate, and mild CHL each lead to a similar decline in the strength of inhibitory synaptic responses in the auditory cortex (Kotak et al., 2008; Mowery et al., 2015; Takesian et al., 2010). The most striking result is that even a transient period of mild hearing loss can induce long-lasting changes to auditory cortex synaptic and membrane properties, but only when the manipulation occurs during a CP (Mowery et al., 2015). Taken together, these results suggest that functional development of the CNS is quite sensitive to a level of sound deprivation that is similar to mild hearing loss.
Figure 3.

Development Hearing Loss, From Profound to Mild, Causes a Decrease in the Strength of Cortical Inhibitory Synapses.

  Development Hearing Loss, From Profound to Mild, Causes a Decrease in the Strength of Cortical Inhibitory Synapses.
Figure 3.

Development Hearing Loss, From Profound to Mild, Causes a Decrease in the Strength of Cortical Inhibitory Synapses.

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Although in vitro electrophysiology experiments confirm that the CNS does change in response to hearing loss, and can tell us much about the underlying cellular mechanisms, they are not able to address how the developing auditory nervous system encodes acoustic cues or how this processing is perturbed by environmental manipulations such as CHL. To address these issues, we have characterized the development of auditory perception and established that permanent CHL can lead to perceptual deficits in adult animals. For example, amplitude modulation (AM) detection thresholds display a prolonged period of maturation, reaching adult-like values near the time of sexual maturation (Sarro & Sanes, 2010, 2011). This is similar to the late development of AM thresholds reported for humans (Banai, Sabin, & Wright, 2011; Hall & Grose, 1994c). When animals are reared with permanent CHL and tested as adults, they display poorer AM detection thresholds and frequency modulation detection thresholds, as compared to age-matched controls (Buran et al., 2014; Rosen, Sarro, Kelly, & Sanes, 2012). Furthermore, auditory cortex processing is also impaired in animals reared with hearing loss. The response of single auditory cortex neurons to AM tones was significantly poorer in CHL animals and the magnitude of the neural deficit matched that of the behavioral differences (Rosen et al., 2012). Thus, a reduction of sensory information can account for limitations to perceptual skills.
If one is to conclude that perceptual deficits are caused by CNS dysfunction, it is necessary to confirm that cochlear function is normal (discussed above; Figure 1). To address this problem, we used the same approach that led us to discover that auditory cortex synapses are vulnerable to mild hearing loss: bilateral earplugs (Caras & Sanes, 2015). Figure 4A summarizes the protocol for these experiments. Animals were reared with bilateral earplugs during an early period of development. However, the earplugs were removed 15 days before behavioral testing. For comparison, we examined a group of animals that experience transient mild hearing loss at a later age. We first confirmed that audiometric thresholds and cochlear function were normal after earplug removal (Figure 4B). As discussed above, an identical period of transient mild hearing loss causes a disruption of auditory cortex cellular properties. For example, we observed a reduced discharge rate evoked by direct injection of current when the manipulation begins during the CP (Figure 4C; Mowery, Kotak, & Sanes, 2015). Fifteen days after earplug removal, animals were tested on an AM detection task. We found that animals reared with earplugs during early juvenile development displayed elevated AM detection thresholds, as compared to age-matched controls (Figure 4D). In contrast, an identical period of transient mild hearing loss at a later age did not impair auditory perception. Thus, animals displayed perceptual deficit even though the peripheral auditory system was functioning normally.
Figure 4.

Mild Hearing Loss During a CP of Development Can Induce Both CNS and Perceptual Deficits.

  Mild Hearing Loss During a CP of Development Can Induce Both CNS and Perceptual Deficits.
Figure 4.

Mild Hearing Loss During a CP of Development Can Induce Both CNS and Perceptual Deficits.

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Taken together, our results suggest that auditory processing deficits persist following a transient period of mild hearing loss because of unremitting changes to CNS cellular properties. This interpretation is strengthened by the observation that peripheral function is normal at the time of behavioral testing. We have not yet recorded the sound evoked responses from auditory cortex neurons as animals perform a psychometric task. Therefore, it will be important to demonstrate that the impaired cellular properties (e.g., Figure 3: inhibitory strength; Figure 4: current-evoked firing rate) recorded in brain slices are correlated with degraded stimulus encoding. Finally, our findings from the transient mild hearing loss model allow us to speculate that CNS deficits also contribute to the diminished perceptual skills that attend permanent sensorineural hearing loss.
Until a few years ago, we would have concluded that the changes to synaptic and membrane properties which attend early hearing loss can explain many of the known behavioral deficits. However, we found that although AM thresholds of earplug-reared juveniles improve during a week of repeated testing, a subset of juveniles continue to display a perceptual deficit (Caras & Sanes, 2015). Similarly, some individuals with a history of hearing loss continue to perform poorly on perceptual tasks long after the average group differences are statistically insignificant (Hall et al., 1995a; Wilmington et al., 1994). Therefore, we have begun to explore CNS mechanisms that could have an impact on task improvement with practice. For example, we have discovered that that the synaptic mechanisms thought to support learning (i.e., long-term potentiation) do not mature properly in the auditory cortex following early hearing loss. This is true for both excitatory and inhibitory synapses (Kotak, Takesian, & Sanes, 2008; Xu et al., 2010). Furthermore, we have recently discovered that hearing loss induces cellular deficits in regions downstream from auditory cortex (Kotak & Sanes, 2014; Mowery, Kotak, & Sanes, 2014). The general implication is that both sensory and nonsensory deficits may contribute to behavioral problems associated with early hearing loss.
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Figure 1.

The Perceptual Deficits That Attend Hearing Loss Can Be Attributable to Peripheral (PNS) or Central Nervous System (CNS) Dysfunction.

  The Perceptual Deficits That Attend Hearing Loss Can Be Attributable to Peripheral (PNS) or Central Nervous System (CNS) Dysfunction.
Figure 1.

The Perceptual Deficits That Attend Hearing Loss Can Be Attributable to Peripheral (PNS) or Central Nervous System (CNS) Dysfunction.

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Figure 2.

Sensorineural Hearing Loss (SNHL) Causes a Decrease in the Strength of Inhibitory Synapses.

  Sensorineural Hearing Loss (SNHL) Causes a Decrease in the Strength of Inhibitory Synapses.
Figure 2.

Sensorineural Hearing Loss (SNHL) Causes a Decrease in the Strength of Inhibitory Synapses.

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Figure 3.

Development Hearing Loss, From Profound to Mild, Causes a Decrease in the Strength of Cortical Inhibitory Synapses.

  Development Hearing Loss, From Profound to Mild, Causes a Decrease in the Strength of Cortical Inhibitory Synapses.
Figure 3.

Development Hearing Loss, From Profound to Mild, Causes a Decrease in the Strength of Cortical Inhibitory Synapses.

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Figure 4.

Mild Hearing Loss During a CP of Development Can Induce Both CNS and Perceptual Deficits.

  Mild Hearing Loss During a CP of Development Can Induce Both CNS and Perceptual Deficits.
Figure 4.

Mild Hearing Loss During a CP of Development Can Induce Both CNS and Perceptual Deficits.

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