Impact of peripheral hearing loss on top-down auditory processing

Abstract

The auditory system consists of an intricate set of connections interposed between hierarchically arranged nuclei. The ascending pathways carrying sound information from the cochlea to the auditory cortex are, predictably, altered in instances of hearing loss resulting from blockage or damage to peripheral auditory structures. However, hearing loss-induced changes in descending connections that emanate from higher auditory centers and project back toward the periphery are still poorly understood. These pathways, which are the hypothesized substrate of high-level contextual and plasticity cues, are intimately linked to the ascending stream, and are thereby also likely to be influenced by auditory deprivation. In the current report, we review both the human and animal literature regarding changes in top-down modulation after peripheral hearing loss. Both aged humans and cochlear implant users are able to harness the power of top-down cues to disambiguate corrupted sounds and, in the case of aged listeners, may rely more heavily on these cues than non-aged listeners. The animal literature also reveals a plethora of structural and functional changes occurring in multiple descending projection systems after peripheral deafferentation. These data suggest that peripheral deafferentation induces a rebalancing of bottom-up and top-down controls, and that it will be necessary to understand the mechanisms underlying this rebalancing to develop better rehabilitation strategies for individuals with peripheral hearing loss.

Top‐down or bottom up: decreased stimulus salience increases responses to predictable stimuli of auditory thalamic neurons

“…Furthermore, repetition-induced increases in speech understanding, as well as improvements in the visual recognition of degraded objects with repetition, provide evidence in support of our interpretation of an increased response to degraded predictable stimuli (Rivenez et al 2006;Muller et al 2013;Helfer et al 2018). Collectively, these results lend support to the hypothesis that less salient stimuli/degraded ascending acoustic code can be compensated for by an increased use of cortical cognitive (experience/contextual) and attentional resources (Bertoli et al 2001;Alain et al 2014;Bidelman et al 2014;Presacco et al 2016a;Lesicko & Llano, 2017).…”

“…The ventral division is lemniscal in nature, projecting principally to layers 3/4, whereas the dorsal and medial subdivisions receive inputs from dorsal and external cortices of the inferior colliculus, tegmentum, superior colliculus and spinal cord considered to be extra-lemniscal and projecting to layers 1 and 6 of the primary auditory cortex, as well as belt areas of the auditory cortex and amygdala, amongst others (Winer et al 2005;de la Mothe et al 2006;Bartlett, 2013). The MGB also receives cholinergic projections that may further engage top-down resources providing cognitive and attentional resources that shape the ascending code (Rouiller & Welker, 1991;Winer et al 2001;Bartlett & Smith, 2002;He, 2003;Bartlett, 2013;Malmierca et al 2015;Guo et al 2017;Lesicko & Llano, 2017;Sottile et al 2017a;Sottile et al 2017b;Schofield & Hurley, 2018). The MGB also receives tectothalamic inputs that carry ascending sensory inputs and shows stimulus-specific adaptation (SSA) to repeating stimuli, facilitating the detection of novel stimuli (Nelken, 2014;Malmierca et al 2015), comprising a property considered to be of bottom-up origin, independent of age and even enhanced by anaesthesia (Ulanovsky et al 2003;von der Behrens et al 2009;Richardson et al 2013a;Malmierca et al 2015;Nir et al 2015).…”

Auditory thalamic circuits and GABAA receptor function: Putative mechanisms in tinnitus pathology

“…However, it should be noted that in both somatosensory and visual systems, considerable plastic expansion in top-down feedback pathways occurs after deafferentation (Djavadian et al, 2001; Fukuda et al, 1984; Garcia del Cano et al, 2002; Jung et al, 2002; reviewed in Lesicko et al, 2016). If there is a deafferentation-induced expansion of the layer 6-derived corticothalamic pathway, for example, this expansion could lead to enhancement or broadening of inhibition derived from the thalamic reticular nucleus.…”

Connectional heterogeneity in the mouse auditory corticocollicular system

“…The classical ascending central auditory pathway begins with the cochlear nucleus (CN), from which the information about sound reaches the superior olivary complex (SOC), followed by the nuclei of the lateral lemniscus (NLL), the inferior colliculus (IC), the medial geniculate body of the thalamus (MGB), and, finally, the auditory cortex (AC) (Malmierca and Ryugo 2012). A prominent feature of the central auditory system is the presence of massive descending connections, which arise virtually at all levels of the auditory pathway (Winer 2005, Bajo, Nodal et al 2007, Bajo, Nodal et al 2010, Terreros and Delano 2015, Lesicko and Llano 2017, Patel, Sons et al 2017). One of these descending pathways, the pathway between the AC and IC, referred to here as the corticocollicular system, has recently garnered much attention due to its potential to alter the sensory information processing at the level of the IC.…”