Sex differences in auditory subcortical function

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Abstract

Objective

Sex differences have been demonstrated in the peripheral auditory system as well as in higher-level cognitive processing. Here, we aimed to determine if the subcortical response to a complex auditory stimulus is encoded differently between the sexes.

Methods

Using electrophysiological techniques, we assessed the auditory brainstem response to a synthesized stop-consonant speech syllable [da] in 76 native-English speaking, young adults (38 female). Timing and frequency components of the response were compared between males and females to determine which aspects of the response are affected by sex.

Results

A dissimilarity between males and females was seen in the neural response to the components of the speech stimulus that change rapidly over time; but not in the slower changing, lower frequency information in the stimulus. We demonstrate that, in agreement with the click-evoked brainstem response, females have earlier peaks relative to males in the subcomponents of the response representing the onset of the speech sound. In contrast, the response peaks comprising the frequency-following response, which encode the fundamental frequency (F0) of the stimulus, as well as the spectral amplitude of the response to the F0, is not affected by sex. Notably, the higher-frequency elements of the speech syllable are encoded differently between males and females, with females having greater representation of spectrotemporal information for frequencies above the F0.

Conclusions

Our results provide a baseline for interpreting the higher incidence of language impairment (e.g. dyslexia, autism, specific language impairment) in males, and the subcortical deficits associated with these disorders.

Significance

These results parallel the subcortical encoding patterns that are documented for good and poor readers in that poor readers differ from good readers on encoding fast but not slow components of speech. This parallel may thus help to explain the higher incidence of reading impairment in males compared to females.

Highlights

► Male and female young adults have measurably different neural responses to speech; to the fast acoustic components of speech, female responses are generally earlier and more robust than male responses. ► The differences observed between males and females in the nervous system’s response to speech parallel those previously reported for poor, relative to good, readers. ► These sex differences provide a baseline for interpreting the higher incidence of language impairment in males, and the neural deficits associated with these disorders.

Introduction

Between the sexes, significant differences exist in the click-evoked auditory brainstem response (ABR), a response predominately representative of high frequency information (Eggermont and Don, 1980). This difference is reflected in the timing of the response, with females having earlier latencies (the time interval between the stimulus onset and the response peak) compared to males (Jerger and Hall, 1980). No sex differences, however, are seen in the phase-locked response to pure tones, a response termed the frequency following response (FFR) that encodes low frequency information (Batra et al., 1986, Hoormann et al., 1992). Because the click- and tone-evoked auditory responses represent the subcortical processing of the elemental components of more complex stimuli, namely onset and phase-locked responses to the acoustic features of speech, (Aiken and Picton, 2008, Akhoun et al., 2008, Basu et al., 2010, Chandrasekaran and Kraus, 2010, Hornickel et al., 2009a, Skoe and Kraus, 2010) we predict that a speech syllable should produce responses that show a non-uniform difference of encoding between the sexes. To address this question, we recorded speech-ABRs to the stop consonant speech-syllable [da] presented to the right ear in a normal learning, young adult population.

Stop consonant syllables, such as [da], have been shown to be difficult for certain populations to perceive, such as individuals with hearing impairments (Gordon-Salant et al., 2007, Townsend and Schwartz, 1981, Van Tasell et al., 1982) and children with specific language impairment and dyslexia (Bradlow et al., 1999, Merzenich et al., 1996, Serniclaes and Sprenger-Charolles, 2003, Tallal, 1980). To determine the biological underpinnings of these deficits, the brainstem response to the stop consonant syllable [da] has been investigated in individuals with speech in noise difficulties (Anderson and Kraus, 2010, Anderson et al., 2010a, Anderson et al., 2010b, Chandrasekaran et al., 2009, Hornickel et al., 2009b), normal hearing young adults (Dhar et al., 2009, Hornickel et al., 2009a, Song et al., 2010, Vander Werff and Burns, 2011), auditory experts (Kraus and Chandrasekaran, 2010, Parbery-Clark et al., 2009a, Parbery-Clark et al., 2009b), typically-developing children, as well as children with reading impairments (Banai et al., 2009, Banai et al., 2005, Chandrasekaran et al., 2009, Cunningham et al., 2001, Hornickel et al., 2009b, Russo et al., 2004, Wible et al., 2004), and children with autism spectrum disorders (Russo et al., 2010, Russo et al., 2008). Although males tend to have a higher prevalence of both autism and language-based learning impairments than females (Katusic et al., 2001, Rutter et al., 2004), and children with autism and language impairments demonstrate impaired subcortical encoding of auditory stimuli (Banai et al., 2009, Banai et al., 2005, Basu et al., 2010, McAnally and Stein, 1996), this is the first study to examine sex differences that are evident in the subcortical response to speech.

Distinct processing for fast and slow (low vs. high frequency) components of acoustic signals has been amply demonstrated (see Zatorre and Gandour, 2008 for review). Acoustic information is asymmetrically routed (Hickok and Poeppel, 2007, Poeppel, 2003) with faster cues lateralized to the left hemisphere (Abrams et al., 2006, Belin et al., 1998, Zatorre and Belin, 2001) and slower information lateralized to the right hemisphere (Abrams et al., 2008, Abrams et al., 2006, Boemio et al., 2005). Because fast, rapid fluctuations are important for conveying linguistic meaning, speech is maximally processed by the left hemisphere (Zatorre et al., 2002). A corresponding right ear advantage (REA) has been demonstrated behaviorally for speech, although this advantage is dependent upon the temporal characteristics of the speech stimulus (Schwartz and Tallal, 1980). Subcortically, lateralization of signal processing is evident, with rapid and transient stimuli being encoded more robustly when presented to the right ear and sustained, slower information being maximally encoded when presented to the left (Ballachanda et al., 1994, Sininger and Cone-Wesson, 2006). The speech-ABR to [da] demonstrates an REA for specific features characteristic of the fast elements of speech (Hornickel et al., 2009a). These differences are also reflected in asymmetry in peripheral processing of auditory stimuli. For example, across both sexes, otoacoustic emissions generated in response to continuous tones are more robust in the left ear, whereas transient stimuli evoke larger responses in the right ear (Sininger and Cone-Wesson, 2004).

Sex differences that exist in the auditory system may interact with peripheral and hemispheric asymmetry for processing slow and fast elements of sound. Regardless of sex, right ears are more sensitive than left to auditory stimuli and females have, on average, greater hearing sensitivity than males (see McFadden, 1998 for review). Moreover, across both sexes, spontaneous otoacoustic emissions (SOAEs) are more prevalent in right ears than left ears but females have larger and more numerous SOAEs than males (Bilger et al., 1990, Lamprecht-Dinnesen et al., 2000). OAEs evoked by transient, rapidly presented stimuli such as clicks or tone bursts (TEOAEs) are also larger in females than males and are generally larger in right than left ears (Ismail and Thornton, 2003, McFadden et al., 2009). Across both sexes, infants demonstrate larger TEOAEs in the right ear while OAEs evoked by continuous tone pairs (DPOAEs) are larger in the left ear (Sininger and Cone-Wesson, 2004). Although adults demonstrate a weak sex difference in the amplitude of DPOAEs, with females having a larger amplitude response, they do not show an ear asymmetry (McFadden et al., 2009).

Given the well-documented sex differences in the auditory system and their interaction with lateralization of auditory processing, we hypothesized that the transient (i.e., fast) aspects of the speech-ABR, like the click-ABR, would be affected by the sex of the subject. Specifically, we predicted that females would have faster response timing for the onset peaks in the speech-evoked response. Furthermore, the lack of a sex effect for the FFR to the fundamental frequency (F0) and second harmonic (Hoormann et al., 1992) of tone burst stimuli led us to hypothesize that males and females would not differ in the encoding of the lowest frequency (i.e., slow) components of the speech syllable or the corresponding temporal interpeak intervals. Because the click-ABR is reflective of primarily high-frequency encoding, we also hypothesized that responses collected from males and females would differ in the spectral magnitude of the higher frequency (i.e., above the F0) information in the stimulus.

Section snippets

Participants

Seventy-six subjects, 38 female, aged 22–29 years (females: mean = 24.21 years, SD = 2.02 years, males: mean = 24.65 years, SD = 2.07 years) were recruited from Northwestern University and reported no history of language impairment. Subjects were included if their air-conduction thresholds were ⩽20 dB nHL at octave frequencies between 250 and 8000 Hz. Inclusion in the study also required that the subject’s wave V latency elicited by a 100-μs click (presented in rarefaction to the right ear at a presentation

Peak timing

Consistent with sex differences reported for the click-evoked ABR, the timing of the onset peaks of the speech-evoked response were sex dependent with females having significantly earlier peak latencies at peaks V (t(75) = 3.496, p = 0.001) and A (t(76) = 3.326, p = 0.001) compared to males (Fig. 2). Timing of the other peaks in the speech-evoked response, when correcting for multiple comparisons, was not dependent on the sex of the subject, including the transition peak C (t(62) = −0.120, p = 0.905), the

Discussion

The purpose of this study was to identify the aspects of the speech-evoked brainstem response of adult subjects that show sex differences. We hypothesized that differences would exist, with females having faster and larger responses than males, and that these differences would be restricted to the encoding of the rapid features of the speech syllable such as the onset of the noise burst and the formant-related frequencies. Indeed, females had significantly earlier encoding of the stimulus onset

Conclusions

This study demonstrated sex differences in the encoding of the fast, but not the slow elements of speech, with females having significantly faster and larger magnitude responses to only the transient aspects of the stimulus compared to males. Although we tested a normal population and cannot speak directly to language impairments, it is interesting that within this population, sex differences in the encoding of a speech stimulus are still apparent. Both the faster timing of the transient peaks

Acknowledgments

The authors thank the members of the Auditory Neuroscience Laboratory, who helped collect the data, and to Dawna Bagherian and Winnie Lin for their help in preparing and processing the data. Thank you to Catherine Warrier, Karen Chan, and Trent Nicol for their comments on a previous version of the manuscript. This work was supported by R01 DC01510.

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