Effect of age on lateralized auditory processing

The lateralization of processing in the auditory cortex varies for different acoustic features. Extracting the meaning of complex sounds for a given task e.g. in speech perception, often requires the simultaneous processing of several fundamental parameters and therefore, an efficient division of labor between the left and right auditory cortex. This in turn requires efficient hemispheric interactions. In older adults, alterations in the lateralization of processing and hemispheric interaction are suggested to interfere with efficient auditory processing.

In older adults, the macro- and microstructure of the corpus callosum is altered (Hasan et al., 2008; Lebel et al., 2010; Ota et al., 2006) and also the white matter integrity of the auditory pathway within hemispheres (Lutz et al., 2007; Profant et al., 2014). For example, fractional anisotropy (FA), a measure of the directionality of diffusion of water molecules, in the corpus callosum decreases during later adulthood (Hasan et al., 2008; Lebel et al., 2010; Sullivan et al., 2010) possibly due to degeneration of fiber tracts. Furthermore, the volume of the corpus callosum decreases in later adulthood (Hasan et al., 2008). It has been shown that variability in the structure of the corpus callosum can influence the interaction between the auditory cortices and the behavior in auditory tasks, e.g. stronger anatomical connection between the superior temporal lobe areas supports better information transfer (Westerhausen et al., 2009). Thus, changes in the structure of the corpus callosum during aging could lead to a decline in hemispheric interaction with aging and therefore, to a decline in processing of auditory stimuli in conditions that require hemispheric interaction (Gootjes et al., 2004; Martin et al., 2005; Westerhausen et al., 2015).

Changes of hemispheric interaction with aging might also have an influence on the lateralization of processing. As the division of labor between the hemispheres may also depend on its advantages and costs (Banich, 1998) a decline in hemispheric interaction during aging might lead to a reduction of lateralized processing because of an increased cost of the hemispheric interaction. The HAROLD (hemispheric asymmetry reduction in older adults) model suggests that activity in the prefrontal cortex during cognitive performance is less lateralized in older adults than in younger adults (Cabeza, 2002). This reduction in laterality can also be seen in other brain areas (Berlingeri et al., 2013) and seems to be similarly present at the stage of early auditory sensory processing (Eddins et al., 2022; Gao et al., 2007) or processing of suprasegmental speech cues (Keller et al., 2019). However, during hearing pink noise, older adults showed a stronger right-lateralized activity in the auditory cortex than younger adults (Profant et al., 2015). Shifts of asymmetry in activity between younger and older adults are also accompanied by changes in performance (Esteves et al., 2021). Older adults show a more symmetric P1-N1 amplitude elicited by syllables and this is accompanied by lower discrimination performance (Bellis et al., 2000). During word repletion, older participants showed a shift of activity asymmetry to the right in the superior temporal gyrus (STG) and Heschl's gyrus compared to the younger participants who showed a left-lateralized asymmetry (Manan et al., 2013). This was accompanied by lower accuracy in the task by older than by younger participants. A change in anatomical asymmetry does not seem to be the reason for functional shifts of asymmetry, since age-related atrophy of the gray matter of the auditory cortex does not change the left lateralized asymmetry of gray matter volume (Profant et al., 2014).

In summary, older adults show several functional and anatomical differences compared to younger adults. However, it is not clear how hemispheric involvement and interaction during the processing of basic acoustic parameters change with aging. The further understanding of these processes could help to better understand deficits of speech processing in older adults. The aim of the present functional magnetic resonance imaging (fMRI) study was to determine the effect of age on hemispheric involvement during two tasks that differently involve the left and right auditory cortex. For this purpose, categorization and sequential comparison of tones based on their direction of frequency modulation (FM) were used. The categorization task mainly involves the right auditory cortex (Behne et al., 2005; Brechmann et al., 2005). The sequential comparison of FM direction additionally involves the left auditory cortex and therefore, requires stronger hemispheric interaction (Angenstein et al., 2013b; Brechmann et al., 2007). The additional recruitment of the left auditory cortex in this task has been explained by working memory processes because the FM direction must be stored for comparison until the next tone is perceived.

Because we expected differences in task performance between older and younger adults, we adjusted the individual task difficulty. It has been shown that task difficulty strongly influences the involvement of the auditory cortex during categorization and comparison of tones according to their FM direction (Brechmann et al., 2005; Brechmann et al., 2019; Brechmann et al., 2007). Therefore, we varied the frequency range of the tones in order to achieve similar task performance between older and younger adults. We used the contralateral noise procedure to determine the lateralization of processing in the auditory cortex (Angenstein et al., 2013a; Angenstein et al., 2013b; Angenstein et al., 2015; Angenstein et al., 2017; Angenstein et al., 2016; Behne et al., 2005; Behne et al., 2006; Brechmann et al., 2019). This method allows determining the involvement of auditory cortex regions largely without an influence of bottom-up caused activity differences that can be expected when using tones with different frequency ranges. In addition, we tested differences between older and younger adults in brain-wide functional connectivity of the auditory cortex. Furthermore, we investigated alterations in interhemispheric anatomical connections due to aging by estimating the integrity of the corpus callosum with diffusion tensor imaging (DTI) data.

In accordance with previous studies, we expected in older adults a reduction in FA, an increase in the mean diffusivity (MD) and a reduction of the corpus callosum size. We tested if there is a different involvement of auditory cortex in task processing in older compared to younger adults despite adapted task difficulty. Such differences can be expected especially for the sequential comparison task because of the required hemispheric interaction and expected reduced anatomical interhemispheric connectivity in older adults.

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