Brief exposure of juvenile rats to noise impairs the development of the response properties of inferior colliculus neurons

Abstract

Temporary impairment of the auditory periphery during the sensitive period of postnatal development of rats may result in a deterioration of neuronal responsiveness in the central auditory nuclei of adult animals. In this study, juvenile rats (postnatal day 14) were exposed for 8 min to intense broad-band noise; at the age of 3-6 months, the excitatory and inhibitory response areas of neurons in the central nucleus of the inferior colliculus were recorded under ketamine-xylazine anaesthesia in these animals and compared with those of age-matched controls. The response thresholds were similar in the exposed and control animals. The frequency selectivity of low-frequency neurons was comparable in both groups; however, high-frequency neurons had significantly wider excitatory response areas in the exposed rats, indicating disrupted development of high-frequency hearing. Forty-one per cent and 25% of neurons in exposed animals and in controls, respectively, lacked a distinct inhibitory area; these neurons had similar frequency selectivity in the exposed and control rats. As the presence of an inhibitory sideband was associated with sharper frequency tuning in both groups, it appears that lateral inhibition substantially influences neuronal frequency selectivity. If present, the inhibitory areas had comparable bandwidths in both groups; however, they were shifted to the side in the exposed animals, allowing the expansion of the excitatory areas. The results indicate that a brief exposure of juvenile rats to noise leads to a significant worsening of the frequency selectivity of inferior colliculus neurons in adult animals; the poorer frequency selectivity may be due to missing or displaced inhibitory sidebands.

Development of vocalization and hearing in American mink (Neovison vison).

“…Our results in mink are comparable to findings in the ferret (Mustela putorious), in which the onset of hearing occurs on postnatal days 26-30 (Morey and Carlile, 1990;Moore and Hine, 1992). In comparison, the rat starts to hear after postnatal days 11-12 (Blatchley et al, 1987;Grécová et al, 2009), with an adult-like ABR developed within days 24-36 (Blatchley et al, 1987). In contrast, adult-like ABR was not acquired in mink within the study period; even at 52days the ABR was neither as large nor as complex as that of the adults.…”

Pulsed Noise Experience Disrupts Complex Sound Representations

“…For example, early exposure to continuous environmental noise has been shown to prolong critical period duration (Chang and Merzenich 2003). Additionally, rearing rats during the first month of life in pulsed white noise disrupts tonotopicity, degrades frequency tuning, and reduces temporal correlation (Grecova et al 2009;Zhang et al 2002). It has also been shown that critical period closure in the auditory cortex (AI) is modulated by sound input dynamics; exposing animals to spectral band-notched noise results in critical period closure for the portion of A1 representing those absent frequencies while exposing animals to band-pass noise kept the critical period open for those frequencies (de Villers-Sidani et al 2007).…”

The effect of noise exposure during the developmental period on the function of the auditory system

“…However, despite several pioneering works that showed the effects of developmental auditory deprivation (Silverman and Clopton, 1977;Clopton and Silverman, 1978;Coleman and O'Connor, 1979) and suggested that an experience-driven activity during ontogeny is necessary for normal development ConstantinePaton, 1983, 1985;Sanes and Tak acs, 1993), it was not until recently that the importance of proper stimulation and patterned neuronal activity was fully appreciated (e.g., Zhang et al, 2001Zhang et al, , 2002Bao et al, 2003;Chang and Merzenich, 2003;Kandler, 2004;Nakahara et al, 2004;Chang et al, 2005;Kandler and Gillespie, 2005;Zhang et al, 2008;Gr ecov a et al, 2009;Bure s et al, 2010Bure s et al, , 2014Bao et al, 2013). It appears that even a short-time detachment of the developing auditory system from natural and rich auditory experience, resulting from an impaired periphery or anomalous stimulation such as noise or clicks, will often result in altered structural and functional characteristics at various levels of the auditory system.…”

“…It appears that even a short-time detachment of the developing auditory system from natural and rich auditory experience, resulting from an impaired periphery or anomalous stimulation such as noise or clicks, will often result in altered structural and functional characteristics at various levels of the auditory system. These changes may comprise, for example, a decrease in the number of hair cells and their ribbon synapses Shi et al, 2015), abnormal dendritic trees and cell sizes of neurons in the central auditory system (Gabriele et al, 2000;Ouda et al, 2014;Lu et al, 2014), altered neuronal responsiveness and representation of stimulus frequency and intensity (e.g., Zhang et al, 2001;Gr ecov a et al, 2009;Bure s et al, 2010;Insanally et al, 2010), or deteriorated psychophysical, behavioral and cognitive functions (Rybalko et al, 2011;Sun et al, 2011;Pan et al, 2011;Rybalko et al, 2015;Suta et al, 2015;RuvalcabaDelgadillo et al, 2015). Despite this volume of work, there still exists great uncertainty as to what effect a specific intervention will have: different interventions may have different consequences at various levels of the auditory system, depending also on the type of intervention, stimulus type, exposure levels, or age of exposure (e.g., Sanes and Constantine-Paton, 1985;Zhang et al, 2001;Chang et al, 2005;Gr ecov a et al, 2009;Insanally et al, 2009;Miyakawa et al, 2013).…”

“…These changes may comprise, for example, a decrease in the number of hair cells and their ribbon synapses Shi et al, 2015), abnormal dendritic trees and cell sizes of neurons in the central auditory system (Gabriele et al, 2000;Ouda et al, 2014;Lu et al, 2014), altered neuronal responsiveness and representation of stimulus frequency and intensity (e.g., Zhang et al, 2001;Gr ecov a et al, 2009;Bure s et al, 2010;Insanally et al, 2010), or deteriorated psychophysical, behavioral and cognitive functions (Rybalko et al, 2011;Sun et al, 2011;Pan et al, 2011;Rybalko et al, 2015;Suta et al, 2015;RuvalcabaDelgadillo et al, 2015). Despite this volume of work, there still exists great uncertainty as to what effect a specific intervention will have: different interventions may have different consequences at various levels of the auditory system, depending also on the type of intervention, stimulus type, exposure levels, or age of exposure (e.g., Sanes and Constantine-Paton, 1985;Zhang et al, 2001;Chang et al, 2005;Gr ecov a et al, 2009;Insanally et al, 2009;Miyakawa et al, 2013). The duration of the insulting exposure plays an important role: for example, a brief intense exposure has often no influence on the hearing thresholds and neuronal excitatory thresholds (Gr ecov a et al, 2009;Kujawa and Liberman, 2009;Bure s et al, 2010;Rybalko et al, 2011;Sanz et al, 2015;Shi et al, 2015), while long-term exposure to moderate-level sounds results in elevated sound thresholds (Gao et al, 2009;Insanally et al, 2010;Lauer and May, 2011).…”