Increasing Cognitive Interference Modulates the Amplitude of the Auditory Brainstem Response

Abstract

Background:

Despite the presence of efferent neural pathways from the cortex to brainstem, evidence for cognitive inhibition and sensory gating on the auditory brainstem has been mixed. Some previous studies have suggested auditory brainstem responses (ABR) can be affected by cognitive load whereas others have not.

Purpose:

The present study explores if the ABR recorded from adults with normal hearing was affected by increased cognitive load involving cognitive interference.

Research Design:

Within-subject repeated measures.

Study Sample:

Twenty young adults with normal hearing (ten females and ten males, aged 21–26 yr).

Data Collection and Analysis:

ABRs were collected with and without cognitive load (a visual Stroop task). Two measures of cognitive interference, that is, the ability to suppress task-irrelevant input, were derived from the performance on the Stroop task.

Results:

No main effect of cognitive load on ABR wave V amplitudes was found. Participants with higher cognitive interference showed increased response times and larger decreases in ABR wave V amplitudes from the no cognitive load to cognitive load conditions.

Conclusions:

The present study showed that ABR wave V amplitudes did not change with increased overall cognitive load (cognitive load with and without cognitive interference), but ABR amplitude was related to cognitive interference. Increased cognitive load in the form of increased cognitive interference could trigger cognitive inhibition and/or sensory gating to suppress the processing of task-irrelevant information at the level of the brainstem. This suppression could present as reduced ABR wave V amplitudes.

Key Words

ABR - accuracy - amplitude - attention - brainstem - cognition - cognitive load - cognitive performance - cognitive resources - normal hearing - response time - Stroop task

INTRODUCTION

Clinical use of the auditory brainstem response (ABR) generally assumes that the ABR is resistant to most cognitive processes. Recent research has challenged this assumption ([Anderson et al, 2013]; [Kraus and White-Schwoch, 2015]) by considering the auditory system as an “integrated whole that interacts with other circuits to guide and refine life in sound” ([Kraus and White-Schwoch, 2015], p. 642). The present study explores this challenge by investigating the relationship between the ABR and cognitive load involving cognitive interference.

Cognitive load refers to “the extent to which the demands imposed by the task at a given moment consume the resources available to maintain successful task execution” ([Pichora-Fuller et al, 2016]). Previous studies have suggested that cognitive load stems from there being a limit to the cognitive resources a person can allocate to solving a task ([Rabbitt, 1968]; [Pichora-Fuller, 2003]; [Ljung et al, 2009a],[b]; [Mattys et al, 2012]; [Rönnberg et al, 2013]; [Pichora-Fuller et al, 2016]; [Brännström et al, 2017]; [von Lochow et al, 2017]). When cognitive load is high (more cognitive resources are engaged to complete a task), cognitive inhibition can occur whereby the cortex acts to suppress task-irrelevant input from lower levels of the brain ([Gorfein and MacLeod, 2007]). Cognitive inhibitory capacity is related to higher-level executive functions, such as the ability to plan, organize, and reason ([Redick et al, 2007]), and to core executive functions such as attention and memory ([Diamond, 2013]). For example, working memory capacity (WMC; [Daneman and Carpenter, 1980]; [Baddeley et al, 1985]; [Baddeley, 2003]), response inhibition, and cognitive flexibility appear to be related to perceptual mechanisms such as perceptual load and attention capture. This, in turn, could influence the degree to which noise affects a person’s cognition ([Sörqvist, 2010]; [Hua et al, 2014a]; [Hua et al, 2014b]; [Stenbäck et al, 2015]).

A possible process within cognitive inhibition is sensory gating. Sensory gating describes the neurological processes that filter out unnecessary or redundant input to the cortex. This is thought to prevent cortical overload by preventing irrelevant information from reaching the cortex. By preventing cortical overload, sensory gating could be a necessary part of task execution ([Diamond, 2013]).

The neural pathways required for cognitive inhibition and sensory gating are present in the efferent auditory nervous system. The efferent auditory system extends from the cortex to the outer hair cells in the cochlea ([Musiek, 1986]). The medial and lateral olivocochlear efferents in the superior olivary complex constitute the last part of this system, and its axons link the superior olivary complex to afferent nerve fibers coming from inner hair cells and to the outer hair cells in the cochlea ([Maison et al, 1999]; [Guinan, 2006]). The auditory cortex influences the superior olivary complex directly or via the inferior colliculus ([Musiek, 1986]; [Thompson and Thompson, 1993]; [Vetter et al, 1993]; [Mulders and Robertson, 2000b]). In animal models, the cochlear potential can be manipulated by applying electrical stimulation of neurons in the auditory cortex or in the inferior colliculus ([Mulders and Robertson, 2000a]; [Xiao and Suga, 2002]). In humans, previous studies using otoacoustic emissions indicate that outer hair cell activity in the cochlea seems to be influenced by cognitive tasks such as selective attention ([Meric and Collet, 1992]; [Giard et al, 1994]; [de Boer and Thornton, 2007]).

Despite the presence of efferent neural pathways from the cortex to brainstem, evidence for cognitive inhibition and sensory gating on the auditory brainstem has been mixed. Some authors have also suggested ABRs can be affected by attention ([Lukas, 1980]; [Bauer and Bayles, 1990]; [Galbraith and Arroyo, 1993]; [Hoormann et al, 1994]; [Galbraith and Doan, 1995]; [Althen et al, 2011]) whereas others have not ([Lukas, 1981]; [Connolly et al, 1989]; [Kuk and Abbas, 1989]; [Hackley et al, 1990]; [Hirschhorn and Michie, 1990]). [Tampas and Harkrider (2006)] reported that females with lower acceptance of background noise (measured as the acceptable noise level; [Nabelek et al, 1991]) while listening to speech demonstrated lower ABR wave V amplitudes. In a study investigating the effects of cognitive load on the ABR, [Sörqvist et al (2012)] found increasing visual working memory load decreased ABR wave amplitudes in adult participants with normal hearing. The largest effect was seen in participants with higher WMC in the condition with the highest WMC load. [Sörqvist et al (2012)] concluded that this was the result of sensory gating whereby the precortical processing of sensory input at the level of the auditory brainstem was modulated by cortical and central task-related mechanisms, that is, neurological processes that filter out redundant or unnecessary input to the brain.

Cognitive interference occurs when the processing of one stimulus feature impedes the simultaneous processing of a second stimulus feature ([Bush et al, 2006]). Perhaps the best known example of cognitive interference is the Stroop effect whereby a participant’s reaction times and error rates increase when reading words that are the names of colors, but those words are printed in colors not denoted by those names (e.g., the word “red” is printed in the color blue) ([Stroop, 1935]). Cognitive interference seems directly involved in auditory processing. Behavioral data suggest that less cognitive interference is related to better speech recognition in noise at more difficult signal-to-noise ratios ([Stenbäck et al, 2016]), and cognitive interference in the visual modality increased when performing the tasks in noise ([Schlittmeier et al, 2015]). Whereas the studies discussed in the previous section suggest that cognitive load could affect the ABR by way of cognitive inhibition and sensory gating, none of those studies directly considered cognitive interference as a measure of cognitive inhibition.

The introduction of cognitive interference to the overall cognitive load could increase any cognitive inhibition and sensory gating effects on the ABR. The present study aimed to investigate this possibility by determining if the ABR recorded from adults with normal hearing was affected by increased cognitive load involving cognitive interference.

METHOD

Twenty-one volunteer participants were conveniently sampled from the Lund University student population and colleagues and friends of the researchers in the Lund region of Sweden. One participant did not complete the ABR testing because of equipment failure at the time of testing. The final 20 participants were 10 females and 10 males, aged 21–26 yr with an average age of 23.3 yrs. All participants self-reported no history of otological disorder and showed pure-tone hearing thresholds ≤20 dB HL for octave frequencies from 250 to 4000 Hz in the test ear. Participants were not screened or questioned regarding attention, memory, or cognitive issues. The Regional Ethics Board in Lund, Sweden, approved the project (approval number 2010/40), and all participants provided written informed consent.

Cognitive Load—Stroop Task

All participants were placed in two conditions: no cognitive load and cognitive load. In the no cognitive load condition, participants were asked to remain awake but restful. In the cognitive load condition, participants were asked to complete a modified visual Stroop task run on a PC using E-Studio 2.0 (E-Prime Professional) and E-Run 2.0 (E-Prime Professional). This modified Stroop task required participants to view black symbols (“1,” “2,” “3,” “4,” or “#”) presented in groups of one to four symbols on a white background on a computer screen ([Bush et al, 2006]). Participants were instructed (verbally and in writing) to count the number of symbols and then press the number key on a wireless keyboard that corresponded to the number of symbols counted. Participants were instructed to respond correctly and as quickly as possible. New trials were presented immediately after participant responses were obtained or if no response was obtained within 4,000 msec of stimulus presentation. One hundred and twenty stimulus trials were presented in a random order. Thirty trials were congruent, 30 were neutral, and 60 were incongruent. Congruent trials contained an amount of number symbols that matched the number symbols used (e.g., “22” or “333”). Neutral trials contained an amount of nonnumber symbols (e.g., “#” or “####”). Incongruent trial contained an amount of number symbols that did not match the number symbols used (e.g., “111” or “44”).

ABR Recordings

Two ABR waveforms were recorded from each participant during both the no cognitive load and cognitive load conditions (where the cognitive load condition consisted of the Stroop task with its randomly presented congruent, neutral, and incongruent trials). The test order of the cognitive load and the no cognitive load conditions was counterbalanced across participants. Two waveforms were recorded in each condition. Left or right ear was randomly selected as the test ear. A single ear was tested because of time constraints. All ABR waveforms were recorded using GSI Audera (version 2.0).

The ABR waveforms were elicited by presenting 70 dBnHL (104 dB peak equivalent SPL [[ISO, 2007]]) tone burst stimuli to the test ear at a rate of 33.1/sec These tone burst stimuli were rarefacting with a center frequency of 3000 Hz, rise and fall times of two periods with Blackmann ramps, and a plateau of one period. 3000 Hz tone bursts were used as they generally generate waveforms with clear morphology at the clinic. Rarefaction was used to avoid any potential ABR amplitude and morphology changes caused by small temporal differences between stimulus presentations ([Don et al, 1994]). Continuous white noise was presented monaurally to the nontest ear at 30 dBnHL. All stimuli were calibrated ([IEC, 2008]) standards using a Brüel and Kjaer type 2636 sound level meter with a type 4144 microphone in a type 4152 artificial ear with a type DB 0138 coupler.

The ABR waveforms were recorded by disposable Neuroline 720 silver/silver chloride electrodes placed on each participant’s high forehead (Fz, noninverting electrode), left and right earlobes (A1 and A2, inverting electrodes for each test ear, respectively), and on the zygomatic bone above the chin (between Lo1 and Io or Lo2 and Io2, common/ground electrode ipsilateral to the test ear). Electrode impedances were verified to be <5 kOhm before and after testing using the GSI Audera (version 2) impedance check function. ABR responses were amplified 200,000 times and high-pass filtered from 30 Hz at −6 dB/octave) and low-pass filtered from 1500 Hz at >40 dB/octave). The ABR responses were recorded using a 30-msec time window and were averaged over 2006 sweeps in the no cognitive load (baseline) condition and from task onset to task completion in the cognitive load (test) condition (which resulted 1530 to 3944 sweeps being averaged depending on the time required to complete the task). A ±25 μV electroencephalogram artifact rejection level was used.

Data Collection and Analysis

For the Stroop task, the number of correct responses and response times were recorded for each of the congruent, neutral, and noncongruent conditions.

Wave V and wave V’ were identified in each participant’s ABR waveform in each condition using expected absolute latencies, and ABR wave V amplitudes were measured from the wave V peak to the wave V’ trough. The ABR wave V amplitudes in each condition were normalized to the average ABR amplitude from all participants across both the no cognitive load and cognitive load conditions. This normalization of ABR wave V amplitudes was done to reduce intersubject variability and to facilitate comparisons between the no cognitive load and cognitive load conditions.

For the Stroop task, descriptive statistics were calculated for the number of correct responses (%) and response times (msec) for correct responses in the congruent, neutral, and incongruent conditions. The Stroop interference values for correct responses and response time were calculated as the value of these measures in the incongruent condition minus their value in the neutral conditions.

Repeated measures analysis of variance (ANOVA) analyses were then conducted on all Stroop measures to verify that the modified Stroop task provided results similar to the results that are usually encountered with the classical Stroop task using color words. In these analyses, one within-subject variable was used (correct responses and response times, respectively), no covariates were used, and Bonferroni corrected post hoc tests were conducted if the ANOVA analyses were significant at the 5% level.

For the normalized ABR wave V amplitudes, descriptive statistics were calculated for the no cognitive load and cognitive load conditions (where the cognitive load condition included the Stroop task with its randomly presented congruent, neutral, and incongruent trials). The within participant difference in normalized ABR wave V amplitudes between the no cognitive load and cognitive load conditions was then described. A paired-samples t-test was then conducted to determine if these ABR amplitude measures differed among the no cognitive load and cognitive load conditions.

Pearson’s correlation coefficient analyses and a partial correlation analysis were conducted to determine any relationships among the ABR wave V amplitude measures and the various Stroop task measures described previously.

RESULTS

Stroop Task

[Table 1] shows the average percentage correct responses and average response times for correct responses in the participants for the congruent, neutral, and incongruent conditions of the Stroop task. A repeated measures ANOVA analyses on the Stroop task results showed a significant main effect for correct responses (Wilks’ lambda = 0.390, F_[2,18] = 14.083, p < 0.001, η² = 0.610). Bonferroni corrected post hoc tests showed that the average correct responses were significantly lower for the incongruent trials compared with both congruent and neutral trials (p < 0.001). A significant main effect was also seen for response times (Wilks’ lambda = 0.438, F_[2,18] = 11.537, p = 0.001, η² = 0.562). All trial types (congruent, neutral, and incongruent) were significantly different from each other in the Bonferroni corrected post hoc analysis (p < 0.001).

Table 1 Average Correct Responses (%) and Response Times (msec) for Congruent, Neutral, and Incongruent Symbols in the Stroop Task. Stroop Interference (Incongruent - Neutral) is also Shown

	Congruent	Neutral	Incongruent	Stroop Interference
Correct responses	99.4 (1.0)	99.8 (2.0)	96.4 (2.9)	2.5 (2.2)
Response times	685 (89)	704 (85)	723 (82)	19 (28)

Notes: Standard deviations are provided within parentheses. N = 20.

ABR Wave V Amplitude and Cognitive Load

[Figure 1] shows an example of individual waveforms with and without cognitive load. A paired-samples t-test of ABR wave V amplitudes between the no cognitive load (mean [M] = 1.05 μV, standard deviation [SD] = 0.39) and cognitive load (M = 0.95 μV, SD = 0.34) conditions showed no significant within-subject effect (t_[19] = 0.923, p = 0.368) (where the cognitive load condition included the Stroop task with its randomly presented congruent, neutral, and incongruent trials).

Figure 1 An example of individual waveforms with and without cognitive load from a single participant. The bottom waveform shows wave V amplitude reduction due to cognitive load.

ABR Wave V Amplitude and Cognitive Interference

Pearson’s correlation coefficient analyses showed a significant correlation (r = 0.581, p = 0.007) between the Stroop interference values for response time in the Stroop task (the response time in the incongruent condition minus the response time in the neutral condition) and the within participant difference in normalized ABR wave V amplitudes between the no cognitive load and cognitive load conditions (M = 0.09, SD = 0.45) (where the cognitive load condition included the Stroop task with its randomly presented congruent, neutral, and incongruent trials). [Figure 2] shows the corresponding data. No significant correlations were observed between any other Stroop task and ABR wave V amplitude measures (r ≤ ±0.387, p ≥ 0.092).

Figure 2 Scatter plot between cognitive interference and the effect of the Stroop task on ABR wave V amplitudes. Note that a score above zero on the y-axis indicates an ABR amplitude decrease for the condition with the cognitive task compared with the no-task condition. A score below zero indicates an ABR amplitude increase for the condition with the cognitive task compared with the no-task condition. The solid line denotes the linear interpolation between the two variables. N = 20.

It was noted that the significant correlation described previously was between two measures that considered cognitive load in different ways. The Stroop interference measure considered cognitive load from the perspective of cognitive interference. This measure was calculated as the difference in scores between two of the conditions in the Stroop task (incongruent and neutral). The ABR wave V amplitude difference measure considered cognitive load from a more general perspective. This measure was calculated from the difference in ABR amplitudes between the no cognitive load and cognitive load conditions. In this calculation, the cognitive load condition included all three conditions in the Stroop task (congruent, neutral, and incongruent).

To account for the Stroop interference (cognitive interference) measure’s use of two of the conditions in the Stroop task (incongruent and neutral) versus the ABR wave V amplitude difference measure’s use of all three conditions in the Stroop task (incongruent, neutral, and congruent), a partial correlation analysis was conducted on these two measures. This analysis controlled for the cognitive load provided by the congruent and the neutral conditions by including the absolute response times for these two conditions as covariates. This partial correlation analysis also showed a significant positive correlation between the Stroop interference values for response time in the Stroop task (the response time in the incongruent condition minus the response time in the neutral condition) and the within participant difference in normalized ABR wave V amplitudes between the no cognitive load and cognitive load conditions (r = 0.614, p = 0.007).

DISCUSSION

The present findings showed ABR wave V amplitudes did not change when overall cognitive load was increased by having the participants complete a Stroop task including congruent, neutral, and incongruent trials. This finding is in contrast to other reports of ABR wave V amplitudes being affected by other general increases in cognitive load such as concurrent visual tasks ([Lukas, 1980]; [Bauer and Bayles, 1990]; [Galbraith and Arroyo, 1993]; [Hoormann et al, 1994]; [Galbraith and Doan, 1995]; [Althen et al, 2011]; [Sörqvist et al, 2012]).

Closer inspection of the present findings showed that participants with greater cognitive interference were more likely to show greater reductions in ABR wave V amplitude with increased overall cognitive load (c.f. [Figures 1] and [2]). This was seen in participants with longer response times in the incongruent versus neutral Stroop test conditions being more likely to show larger reductions in ABR wave V amplitudes when overall cognitive load was increased by having the participants complete a Stroop task including congruent, neutral, and incongruent trials.

A relationship between cognitive interference and changes in ABR wave V amplitude with increased cognitive load could be related to attention and/or memory capacity. As cognitive interference increases, so could the load on attention and/or working memory. This, in turn, could trigger cognitive inhibition and/or sensory gating in an attempt to suppress task-irrelevant information in the brainstem. An effect of such suppression could be a reduced ABR wave V amplitude. Any such suppression could be complicated by other interactions between a participant’s cognitive (attention and/or memory) capacity and cognitive interference. Such complexities were suggested by [Sörqvist et al (2012)] who demonstrated that an increasing amount of working memory load decreased ABR wave amplitudes more than conditions with lesser load, and individuals with higher WMC reduced their ABR responses more in the condition with the highest working memory load. [Sörqvist et al (2012)] argued that the efficiency of sensory gating was related to the individual’s WMC where those with higher WMC had more efficient sensory gating than those with lower WMC. Put another way, [Sörqvist et al (2012)] argued that participants with higher WMC showed greater cognitive inhibition and/or sensory gating either because they have the cognitive resources available to do so or because they have a more efficient sensory gating mechanism. In a larger perspective, the modulation of brainstem auditory processing by cognitive interference may provide insight into the neurological processes that filter out unnecessary or redundant input to the cortex. This may prove important when understanding, for example, speech perception in adverse listening conditions.

From a clinical perspective, the present study’s findings suggest two possibilities. First, the potential for cognitive load to reduce ABR wave V amplitude in participants with greater cognitive interference supports the need to reconsider the general assumption that the ABR is resistant to most cognitive processes. It also supports recent calls to reconsider the auditory system as an “integrated whole that interacts with other circuits to guide and refine life in sound” ([Kraus and White-Schwoch, 2015], p. 642). Second, if further research shows the present study’s relationship between the ABR and cognitive interference to be robust, then new clinical ABR protocols could be developed to identify the levels of cognitive interference in individual patients/clients. Such new ABR protocols could support efforts to better manage hearing loss and cognitive decline in aging populations by identifying those with hearing loss plus increased cognitive interference versus those with hearing loss alone. In light of these possibilities, further research into the clinical implications of any relationships between the ABR and cognitive interference is warranted.

The present study’s findings had several limitations. First, the comparison of ABR wave V amplitudes with and without overall cognitive load was not able to rule out a potential effect of cognitive interference on ABR amplitude. ABR wave V amplitudes may have been reduced in the incongruent Stroop condition only, but this effect could have been masked when the ABR was averaged across all Stroop conditions (congruent, neutral, and incongruent) used to increase overall cognitive load. Future studies should record the ABR for congruent, neutral, and incongruent conditions separately. Second, the observed relationship between cognitive interference and changes in ABR wave V amplitude with increased cognitive load was partly confounded by the derived nature of the measures identified in this relationship. In particular, the measure of cognitive interference used two of the conditions in the Stroop task (incongruent and neutral) whereas the change in ABR wave V amplitude with overall cognitive load used all three conditions in the Stroop task (incongruent, neutral, and congruent). This confound was partly mitigated by the observed relationship remaining after a reanalysis that controlled for the cognitive load provided by the congruent and the neutral conditions in the Stroop task. The interpretation of the present findings is also influenced by the uneven number of stimulus trials used. We chose to increase the number of incongruent trials as the focus of the present study was to examine cognitive interference which only occurs for the incongruent trials. A second reason is that the error rate increases for incongruent stimuli which means that erroneous trials have to be removed when calculating response times. We increased the number of incongruent trials to mitigate this limitation. In future studies, it would also be beneficial if participants were screened or questioned regarding attention, memory, or cognitive issues as wave V suppression could be influenced by a subjective cognitive capacity and cognitive interference.

CONCLUSIONS

The present study’s results showed that ABR wave V amplitudes did not change when overall cognitive load was increased, but that participants with greater cognitive interference were more likely to show greater reductions in ABR wave V amplitude with increased overall cognitive load. These results suggest that increased cognitive load in the form of increased cognitive interference could trigger cognitive inhibition and/or sensory gating to suppress the processing of task-irrelevant information at the level of the brainstem. This suppression could present as reduced ABR wave V amplitudes.

Abbreviations

ABR: auditory brainstem response

ANOVA: analysis of variance

M: mean

SD: standard deviation

WMC: working memory capacity

No conflict of interest has been declared by the author(s).

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