Attentional Modulation of the Inner Ear: A Combined Otoacoustic Emission and EEG Study

Abstract

Attending to a single stimulus in a complex multisensory environment requires the ability to select relevant information while ignoring distracting input. The underlying mechanism and involved neuronal levels of this attentional gain control are still a matter of debate. Here, we investigated the influence of intermodal attention on different levels of auditory processing in humans. It is known that the activity of the cochlear amplifier can be modulated by efferent neurons of the medial olivocochlear complex. We used distortion product otoacoustic emission (DPOAE) measurements to monitor cochlear activity during an intermodal cueing paradigm. Simultaneously, central auditory processing was assessed by electroencephalography (EEG) with a steady-state paradigm targeting early cortical responses and analysis of alpha oscillations reflecting higher cognitive control of attentional modulation. We found effects of selective attention at all measured levels of the auditory processing: DPOAE levels differed significantly between periods of visual and auditory attention, showing a reduction during visual attention, but no change during auditory attention. Primary auditory cortex activity, as measured by the auditory steady-state response (ASSR), differed between conditions, with higher ASSRs during auditory than visual attention. Furthermore, the analysis of cortical oscillatory activity revealed increased alpha power over occipitoparietal and frontal regions during auditory compared with visual attention, putatively reflecting suppression of visual processing. In conclusion, this study showed both enhanced processing of attended acoustic stimuli in early sensory cortex and reduced processing of distracting input, both at higher cortical levels and at the most peripheral level of the hearing system, the cochlea.

Evidence against attentional state modulating scalp-recorded auditory brainstem steady-state responses

“…This resulted in the randomization of relative onset timings of digits across ears when stimuli were presented dichotically. Furthermore, given that previous reports of modality-specific attentional modulation of subcortical responses are more consistent than reports of modulation due to selective, within-modality attention shifts (e.g., Lukas, 1980; Oatman and Anderson, 1980; Lukas, 1981; Bauer and Bayles, 1990; Galbraith et al, 2003; Delano et al, 2007; Wittekindt et al, 2014), we also introduced an additional condition in which participants attended to visual stimuli while ignoring monaurally presented auditory stimuli. The detection task employed in the second experiment was similar to the task utilized in Experiment 1 (detect two consecutive, increasing digits in the attended ear or, for the visual task, on a computer monitor), but with a small financial bonus contingent on performance levels to encourage participants’ maximum engagement with the task.…”

“…“Inter-modal” selective attention (e.g., paying attention to visual stimuli while ignoring simultaneously presented auditory stimuli) has also been shown to modulate the strength of cortical auditory responses. Specifically, the magnitude of the AEP (Hackley et al, 1990; Choi et al, 2013) and ASSR (ASSR; Wittekindt et al, 2014) both have been observed to increase when subjects are actively listening for an auditory stimulus compared to when they perform a visual task and are ignoring the same auditory inputs.…”

“…This is especially true given the observation of subcortical attentional effects using other types of functional measurements of subcortical auditory processing, including otoacoustic emissions (OAEs; Giard et al, 1994; Maison et al, 2001; Wittekindt et al, 2014) and fMRI BOLD responses in IC (Rinne et al, 2008). …”

Medial olivocochlear efferent reflex inhibition of human cochlear nerve responses

“…Indirect measurements of MOC inhibition have been made psychophysically (e.g., Kawase et al 2000; Aguilar et al 2013; Wicher & Moore 2014; Strickland 2001, 2004, 2008; Wojtczak et al 2014; Jennings et al 2009; Roverud & Strickland 2010; Yasin et al 2014). But, psychophysical measurements are confounded by the possibility that the MOC reflex, the sound used to elicit MOC reflex, or the attention required for the psychophysical measurements, may change signal processing in the brain as well as in the cochlea (Keefe et al 2009; Wittekindt et al 2014). To understand the roles of the MOC reflex in human hearing, it is necessary to know the extent to which the MOC reflex inhibits responses from the cochlear nerve and to do this direct measurements of cochlear-nerve responses are needed.…”

Efferent modulation of pre-neural and neural distortion products

“…Simultaneously recorded OAEs and neural responses provide promise for understanding functional efferent effects (Elsisy & Krishnan, 2005, 2008; Wittekindt et al, 2014; Mertes & Leek, 2016). In future experiments, we plan to simultaneously record DPOAEs and FFRs (e.g., Elsisy & Krishnan, 2005, 2008) using small frequency steps or swept tones to account for DPOAE fine structure and to obtain FFR spectra with sufficient resolution for unambiguous phase delay estimates.…”