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.

Figure 1

Schematic diagram illustrating subcortical top-down projections across the five sensory systems. Black arrows = bottom-up projections. Blue arrows = top-down projections. CN = cochlear nuclei, DCN = dorsal column nuclei, IC = inferior colliculus, LGN = lateral genicular nucleus, MGB = medial geniculate body, NLL = nuclei of the lateral lemniscus, NTS = nucleus tractus solitarius, PAG = periaqueductal gray, PBN = parabrachial nuclei, SC = superior colliculus, SO = superior olive, VPL = ventral posterior lateral nucleus of thalamus, VPM = ventral posterior medial nucleus of thalamus.

Figure 2

Psychometric curve illustrating the improvement in speech intelligibility when words in noise are given in context. This improvement is seen as a shift to the left of the psychometric curve (obtained with permission from Miller et al. 1951).

Figure 3

Intelligibility (in rationalized-arcsine-unit, or RAU, scores) vs. signal to noise (SNR) in cochlear implant (CI) users and normal hearing users listening to noise-vocoded speech (NHCI). Sound is presented as either intact (VU, or Vrij University, baseline in black) or degraded, retaining 75% duty cycle (blue) or 50% duty cycle (red). Sounds are presented either with silence in the gaps (rightmost part of x- axis) or noise with varying SNR (leftmost part of x-axis). Asterisk = p < 0.05. (obtained with permission from (Bhargava et al., 2014)).

Figure 4

Layer-specific functional organization of the auditory cortex in normal (left) and congenitally deaf white cats (right). Intracortical transmission deficits in the congenitally deaf white cat likely affect corticofugal pathways in addition to callosal and hierarchical cortico-cortical networks (obtained with permission from (Kral et al., 2007)).

Figure 5

A) Terminal field of a control rat. B) Expanded terminal field of rat enucleated in early postnatal life. C) Terminal field of rat enucleated in adulthood, demonstrating a lack of expansion (obtained with permission from (García Del Caño et al., 2002)). SG = stratum griseum superficiale, SO = stratum opticum, SZ = stratum zonale.