Research paperConsequences of unilateral hearing loss: Cortical adjustment to unilateral deprivation
Introduction
Electrophysiological investigations of conductive hearing loss (CHL) in animals have shown that CHL changes the way sound is processed in the peripheral and central auditory system (e.g., Clopton and Silverman, 1978, Webster and Bobbin, 1986, Sumner et al., 2005, Xu and Jen, 2001, Jen and Xu, 2002, Xu et al., 2007). Centrally, unilateral CHL results in a decrease in glucose uptake as measured by the 2-deoxyglucose (2-DG) method, affecting cellular activity and metabolism in the major afferent projection from the manipulated ear (e.g., Tucci et al., 1999, Tucci et al., 2001). In these animals, unilateral CHL produced by malleus removal changes the pattern of 2-DG uptake across auditory brainstem structures in a manner similar to animals that have severe cochlear damage, i.e., damage that results in a profound hearing loss.
Using a different paradigm to produce unilateral CHL (surgical atresia), Stuermer and Scheich (2000) demonstrated enhanced 2-DG uptake in primary auditory cortex (AI) but not the anterior auditory field (AAF) contralateral to the manipulated ear. In that study, gerbils’ ears were closed from postnatal day 9 (P9) until testing and sacrifice at P27. Since the onset of hearing in gerbils is approximately P12 (Finck et al., 1972, Woolf and Ryan, 1984, Ryan and Woolf, 1993), the manipulated ear never received normal stimulation after hearing onset. Pienkowski and Harrison (2005) demonstrated that in chinchilla, a precocious species with onset of hearing in utero, many basic features of auditory cortex are functional at P3 (e.g., sensitivity, firing rates, tonotopic map), yet the spectral–temporal response properties of cortical neurons continue to develop beyond P30 and into adulthood. These authors suggest that it is the postnatal acoustic environment, with its more complex sound content, that is ultimately responsible for proper cortical development.
Enhanced cortical activity has also been show to occur, at least transiently, in adult animals subsequent to chemical ablations of the cochlea (e.g., Popelar et al., 1994, Qiu et al., 2000), and partial mechanical destruction of the cochlea induces re-organization of frequency representations in the contralateral auditory cortex of adult animals (e.g., Robertson and Irvine, 1989, Rajan et al., 1993). Furthermore, neurons in auditory cortex alter their response properties subsequent to changes in stimulus pairings involved in learning and attention paradigms (e.g., Recanzone et al., 1993, Kilgard et al., 2007, Weinberger, 2007, Zatorre, 2007).
Until recently, AI and AAF were considered to be, in essence, mirror images of one another, each possessing a strict and orderly tonotopic map (e.g., Merzenich et al., 1975, Knight, 1977, Reale and Imig, 1980, Phillips and Irvine, 1982, Morel et al., 1993, Thomas et al., 1993, Stiebler et al., 1997, Rutkowski et al., 2003) and having similar anatomical connections (e.g., Anderson et al., 1980b, Imig and Reale, 1980, Imig and Morel, 1983), though AAF occupies a smaller area of cortex. This concept has been challenged in several species, based on anatomical, behavioral, and physiological evidence. For example, in cat, there are differences in the proportion of thalamic and cortical inputs to AI and AAF (e.g., Morel and Imig, 1987, Lee et al., 2004a, Lee et al., 2004b), deactivation of AI (but not AAF) disrupts performance on sound localization tasks (Jenkins and Merzenich, 1984, Lomber et al., 2007), and neurons of AI and AAF differ in their response to temporally modulated stimuli (amplitude or frequency modulated tones; Schreiner and Urbas, 1988, Tian and Rauschecker, 1994). Although responses to frequency-modulated tones can be used to differentiate AI from other regions of auditory cortex in gerbil, it does not serve to distinguish AI from AAF (Schulze et al., 1997). Other studies indicate that AI and AAF serve different roles in processing complex sounds (e.g., Linden et al., 2003, Imaizumi et al., 2004, Takahashi et al., 2005), suggesting that AAF may be specialized for rapid temporal processing (Linden et al., 2003). Presumably this specialization requires natural acoustic experience, and that normal development of auditory cortex is dependent upon the postnatal acoustic environment (Takahashi et al., 2006).
The studies mentioned above, and others, point to the differing nature of changes that can occur in the central auditory system though developmental versus adult forms of “plasticity” as a function of either peripheral or central processing mechanisms (see Calford, 2002, Syka, 2002, Irvine, 2007). In our previous reports we investigated the effects of unilateral hearing loss, typically induced in gerbils at P21 after the ear has gained some measure of acoustic “experience”, within nuclei of the auditory brainstem. Here we extend our studies to include the effect of CHL and cochlear ablation (CA) on the medial geniculate (MG) and auditory cortex (AI and AAF). For the present study, we measured glucose metabolism by the 2-DG method in animals 3 weeks after a unilateral CHL was produced by malleus removal, or after a unilateral CA in P21 gerbils. These results were compared to an anesthesia only sham group (SH) at P42. For comparison with our previous studies, we also measured glucose uptake by the inferior colliculus (IC), and in the medial geniculate (MG) in the same animals. Our primary goal was to address the question of how unilateral CHL effects metabolic activity in the contralateral auditory cortex of immature animals that have experienced approximately 10 days of normal binaural development.
Section snippets
Subjects
Eighteen Mongolian gerbils (Meriones unguiculatus), obtained from a commercial supplier (Charles Rivers), were used in this study. All anesthetic, operative, and postoperative procedures and care followed NIH guidelines, and were approved by the Institutional Animal Care Committee. All experimental procedures and tissue preparation was conducted at the University of Kansas Medical Center. Densitometry and tissue analysis was done at the Duke University Medical Center.
Each animal entered this
Results
We used uptake of 2-DG as a tool to measure activity within the auditory midbrain and forebrain of young gerbils 3 weeks after a unilateral hearing loss produced by middle (conductive) or inner (sensorineural) ear manipulation. We found significant left–right (ipsilateral–contralateral) differences between the IC’s subsequent to either manipulation, and the activity in contralateral IC differed significantly from SH in both conditions. No significant change in glucose uptake was observed in the
Discussion
Overall the results of this study conform to our earlier investigations, showing that unilateral CHL (and CA) significantly reduce glucose activity in the contralateral IC (e.g., Tucci et al., 1999). At the level of auditory cortex, CHL significantly reduces activity in the contralateral AAF. This suggests that conductive impairment does have a measurable effect on auditory cortex, and thus may contribute to potential cognitive dysfunctions related to processing sounds and speech. To explain
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2017, Hearing ResearchCitation Excerpt :In addition, these studies investigated changes in neural activity after noise trauma (Dong et al., 2010; Salvi et al., 1990). However, there are deprivation studies (involving transient conductive hearing loss) in animals that have shown effects that are consistent with the ABR findings in the present study (Hutson et al., 2008, 2009). For example, Hutson et al. (2009) reported a significant reduction in neural activity in adult gerbils (as measured by 2-deoxy-glucose uptake) 1 week after mild unilateral conductive hearing loss (removal of the malleus), in the afferent auditory pathway relative to the affected ear.
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2014, NeuroscienceCitation Excerpt :Cortical-evoked thresholds returned to levels similar to those for controls in a subgroup of deprived animals after 3 weeks of exposure to ambient noise following the 8 months of deprivation. Studies investigating physiological modifications in monaural deprivation have found decreases in 2-deoxycglucose (2-DG) uptake in the deprived ear pathway, including the anteroventral cochlear nucleus (AVCN), IC, MG, AI, and anterior auditory field (AAF) compared to control animals, but no alteration in the medial superior olive (MSO) (Hutson et al., 2008, 2009) (see Table 3). Glucose utilization in the auditory pathway of the open ear (contralateral to the deprived ear) has shown a different pattern, with decrease in the IC, MG and AI, more utilization in the MSO, and no modification in the AVCN and AAF (see Table 3).
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2009, Physiology and BehaviorCitation Excerpt :The peripheral auditory system [25,26] and many aspects of central auditory processing [27,28] are well described. Gerbils are frequently used in developmental studies [29,30], in studies investigating hearing loss [31] and regeneration [32,33]. Gerbils have also been investigated for general aspects of domestication as two different strains are available: the domesticated strain commonly used in laboratory research, and a strain descending from wild-type gerbils captured in 1995.