Postnatal development of auditory central evoked responses and thalamic cellular properties

Abstract

During development, the sense of hearing changes rapidly with age, especially around hearing onset. During this period, auditory structures are highly sensitive to alterations of the acoustic environment, such as hearing loss or background noise. This sensitivity includes auditory temporal processing, which is important for processing complex sounds, and for acquiring reading and language skills. Developmental changes can be observed at multiple levels of brain organization-from behavioral responses to cellular responses, and at every auditory nucleus. Neuronal properties and sound processing change dramatically in auditory cortex neurons after hearing onset. However, development of its primary source, the auditory thalamus, or medial geniculate body (MGB), has not been well studied over this critical time window. Furthermore, to understand how temporal processing develops, it is important to determine the relative maturation of temporal processing not only in the MGB, but also in its inputs. Cellular properties of rat MGB neurons were studied using in vitro whole-cell patch-clamp recordings, at ages postnatal day (P) 7-9; P15-17, and P22-32. Auditory evoked potentials were measured in P14-17 and P22-32 rats. MGB action potentials became about five times faster, and the ability to generate spike trains increased with age, particularly at frequencies of 50 Hz and higher. Evoked potential responses, including auditory brainstem responses (ABR), middle latency responses (MLR), and amplitude modulation following responses, showed increased amplitudes with age, and ABRs and MLRs additionally showed decreased latencies with age. Overall, temporal processing at subthalamic nuclei is concurrently maturing with MGB cellular properties.

Differential maturation of vesicular glutamate and GABA transporter expression in the mouse auditory forebrain during the first weeks of hearing

“…On average, the size of GABAergic terminals in the MGB were qualitatively smaller than excitatory (VGluT2-ir) terminals from the IC, but there does not appear to be a definitive way to distinguish GABAergic terminal populations from the thalamic reticular nucleus (TRN) and IC based on morphology (Bartlett et al 2000). Their delineation would be of interest for future anatomical studies, and may serve to support recent neurophysiological studies that have focused on maturation of excitatory and inhibitory properties in the MGB during postnatal development (Venkataraman and Bartlett 2013, 2014). …”

“…One notable exception can be found in the cortical sensitivity to airborne tone bursts, which increases 100-fold (i.e., 40 dB) between P11 and P14 in accordance with the commensurate maturation of ear canal patency and cochlear biomechanics that also unfold during this brief period (Adise et al 2014; Mikaelian et al 1965; Mills and Rubel 1998). However, the dynamic expression levels of VGluT1, VGluT2, and VGAT in conjunction with changes in the intrinsic membrane properties (Metherate and Cruikshank 1999; Oswald and Reyes 2011) and ligand-gated receptor composition (Hsieh et al 2002; Venkataraman and Bartlett 2013, 2014) in the auditory forebrain between P11 and P14 suggest that the rapid maturation of sound-evoked responses measured in A1 and MGB of intact animals during the first days of hearing may reflect a combination of peripheral and central changes.…”

“…However, many other developmental milestones for changes in protein expression and neurophysiological responses around the onset of hearing have been established, which provide context for the present studies. The delayed onset of hearing in altricial animals has provided researchers with a convenient window to study activity-dependent changes in basic neuronal response properties (Barkat et al 2011; Brown and Harrison 2010; Carrasco et al 2013; Chang et al 2005; de Villers-Sidani et al 2007; Insanally et al 2010; Kral et al 2005; Mrsic-Flogel et al 2003, 2006; Polley et al 2013; Razak and Fuzessery 2007; Rosen et al 2010; Sarro et al 2011; Trujillo et al 2013) and associated mechanisms (Dorrn et al 2010; Metherate and Cruikshank 1999; Oswald and Reyes 2008, 2011; Venkataraman and Bartlett 2013, 2014). Critical periods for sound processing are also contained within this window (Barkat et al 2011; Fitch et al 2013; Froemke and Jones 2011; Keating and King 2013; Kral et al 2013; Polley et al 2013; Sanes and Bao 2009; Sanes and Kotak 2011; Sanes and Woolley 2011; Takesian et al 2009; Whitton and Polley 2011).…”

Development of subcortical speech representation in human infants

“…These findings are supported by morphological evidence that the organ of Corti develops prior to birth (Lavigne-Rebillard and Pujol, 1987). Evidence from evoked potentials, however, indicates that the central auditory system continues to mature into school-age years and adolescence in human Kushnerenko et al, 2002;Johnson et al, 2008;Sussman et al, 2008;Choudhury and Benasich, 2011;Marcoux, 2011;Mahajan and McArthur, 2012;Skoe et al, 2013) and in animal models (Venkataraman and Bartlett, 2013a), with the prominence of specific cortical peaks changing with age (Ponton et al, 2000). Observed changes include earlier latencies, decreased response variability, and increased response magnitude of subcortical and cortical components.…”

“…In developing rats, agerelated changes occur in the properties of IC inhibition and in GABAergic projections to the medial geniculate body (MGB) of the thalamus (Venkataraman and Bartlett, 2013b). The time course of these changes is similar to that of the development of temporal coding, as assessed by evoked potentials, in developing young rats (Venkataraman and Bartlett, 2013a). Given the results from the Venkataraman and Bartlett studies, the changes in offset peak properties may arise from changes in inhibitory neurotransmission affecting the ability to precisely encode duration of auditory stimuli.…”