Mapping hemispheric symmetries, relative asymmetries, and absolute asymmetries underlying the auditory laterality effect
Introduction
Functional differences between the two cerebral hemispheres represent a basic characteristic of the human brain (Hervé et al., 2013). In healthy participants these differences have been traditionally studied using behavioral paradigms which are constructed to selectively assess the processing abilities of each hemisphere. One of the most frequently used paradigms is dichotic listening, which is commonly used to behaviorally assess hemispheric asymmetries for speech and language processing (Bryden, 1963, Hugdahl, 2011, Kimura, 1961, Kimura, 2011). The paradigm typically consists of the presentation of two slightly differing verbal stimuli (such as consonant–vowel syllables), whereby one stimulus is presented to the left ear and the other one is simultaneously presented to the right ear. Instructed to report the syllable that was perceived best, participants more often report the right- than the left-ear stimulus. This behavioral auditory laterality effect is widely accepted to be a non-invasive indicator of left-hemispheric dominance for speech and language processing (e.g., Della Penna et al., 2007, Kimura, 1967, Tervaniemi and Hugdahl, 2003, Toga and Thompson, 2003); an interpretation which has been validated in studies on patients with hemispheric or callosal lesions (e.g., Eslinger and Damasio, 1988, Hugdahl and Wester, 1992, Pollmann et al., 2002, Spierer et al., 2007) as well as in clinical studies using the invasive sodium-amytal procedure (e.g., Hugdahl et al., 1997, Kimura, 1961, Zatorre, 1989).
At the same time, functional neuroimaging studies in healthy participants also indicate that the task is more complex since both hemispheres are usually reported to be significantly activated when performing a dichotic-listening task. More specifically, bilateral frontal and temporal brain regions are found to be activated, irrespective of whether the dichotic-listening condition was contrasted with silence (e.g., Dos Santos Sequeira et al., 2010, Stefanatos et al., 2008, van den Noort et al., 2008), binaural verbal (e.g., Jäncke and Shah, 2002, Lipschutz et al., 2002, Thomsen et al., 2004), or non-verbal control condition (e.g., Hugdahl et al., 1999). However, significant activation of both hemispheres does not exclude that one hemisphere is more strongly activated than the other, i.e. showing a relative asymmetrical activation pattern. To date, no study has systematically analyzed both symmetries as well as relative and absolute asymmetries in brain activation in response to the dichotic-listening paradigm. This would allow distinguishing between symmetrically engaged brain networks that possibly are responsible for processing of basic acoustic features of the stimulus and response execution, and asymmetrically engaged brain areas that are possibly responsible for the observed behavioral laterality effects.
Although functional imaging allows to directly assess hemispheric asymmetries (e.g., Badzakova-Trajkov et al., 2010, Josse et al., 2008, Kompus et al., 2011, Pujol et al., 1999, Westerhausen et al., 2006), some important issues need to be considered when conducting the asymmetry analysis. As pointed out frequently, demonstrating that a brain region in one hemisphere is significantly engaged while its contralateral counterpart is not, provides only insufficient evidence for hemispheric asymmetry (e.g., Friston, 2003, Liégeois et al., 2002; or for a more general discussion see Nieuwenhuis et al., 2011). Rather, it could be the case that the activation differences in both hemispheres are of more or less of same magnitude, but just above the statistical threshold in one hemisphere and just below the threshold in the other. Likewise, showing that both hemispheres are significantly activated does not exclude that there is an asymmetry in the magnitude of the activation between the hemispheres. Thus, a direct inter-hemispheric comparison of the activation is required in order to test for hemispheric asymmetries. Testing for inter-hemispheric differences alone ignores the level of activation within each hemisphere, and only when supplemented with further analyses, regions that show absolute and relative asymmetry, respectively, can be distinguished. Here, absolute asymmetry is defined as a significant inter-hemispheric difference together with the task-related contrast only being significant in one of the two compared regions. In case of a relative asymmetry both homologue regions show a significant effect but one is activated significantly stronger than the other (for overview see Table 1).
We report an analysis of a large-scale fMRI study on 104 participants, for the first time combining an interhemispheric asymmetry and conjunction analysis to assess symmetries as well as relative and absolute asymmetries during dichotic listening. For this purpose, the paradigm was implemented as closely matching to the standard version of the paradigm as it is typically used in behavioral laterality studies in many research laboratories and clinical units (Hugdahl, 2003, Hugdahl et al., 2009). This approach enabled us to study functional hemispheric symmetries and asymmetries that parallel behavioral auditory laterality measures.
Section snippets
Participants
The sample consisted of 104 healthy, right-handed participants between 18 and 45 years old (mean: 28.5 ± 7.2 years), of whom 49 were females and 55 were males. The data of six additionally recruited left-handed subjects was excluded in order to increase the homogeneity of the sample, whereby handedness was verified with a Norwegian version of the Raczkowski's questionnaire (Raczkowski et al., 1974). All participants were native Norwegian speakers and had no psychiatric or neurological history.
Behavioral data
The mean correct right and left ear report was 47.0% (SD: 12.9) and 31.8% (SD: 11.7), respectively, yielding a behavioral right ear advantage of LI = 19.1% (SD: 26.0). Accordingly, errors – i.e., reporting a syllable that was not presented – occurred in 21.2% (SD: 13.3%) of the trials. Both direct comparison of left- and right-ear performances (paired t-test: t(206) = 8.91, p < 0.0001, d = 0.73) as well as testing of the mean LI score for significance (t-test against 0: t(104) = 7.52, p < 0.0001, d = 0.73)
Discussion
Although previous studies have studied brain activation during dichotic-listening performance (e.g., Hugdahl et al., 1999, Jäncke and Shah, 2002, Lipschutz et al., 2002, Stefanatos et al., 2008, Thomsen et al., 2004), we here for the first time identify brain areas which are activated symmetrically, and distinguish between brain regions that show a relative and absolute asymmetry. The results can be summarized in two points. First, superior temporal, lateral and medial frontal and inferior
Acknowledgments
Funding for this study was provided by European Research Council (ERC, VOICE 249516; advanced grant to Kenneth Hugdahl).
References (85)
- et al.
The somatotopy of speech: phonation and articulation in the human motor cortex
Brain Cogn.
(2009) - et al.
Corpus callosum morphometry and dichotic listening performance: individual differences in functional interhemispheric inhibition?
Neuropsychologia
(1993) - et al.
Conjunction revisited
Neuroimage
(2005) - et al.
Hemispheric differences in auditory oddball responses during monaural versus binaural stimulation
Int. J. Psychophysiol.
(2009) - et al.
The integration of large-scale neural network modeling and functional brain imaging in speech motor control
Neuroimage
(2010) - et al.
Corpus callosum size correlates with asymmetric performance on a dichotic listening task in healthy aging but not in Alzheimer's disease
Neuropsychologia
(2006) - et al.
Revisiting human hemispheric specialization with neuroimaging
Trends Cogn. Sci.
(2013) - et al.
Sex differences in language asymmetry are age-dependent and small: a large-scale, consonant–vowel dichotic listening study with behavioral and fMRI data
Cortex
(2013) Fifty years of dichotic listening research — still going and going and …
Brain Cogn.
(2011)- et al.
The “forced-attention paradigm” in dichotic listening to CV-syllables: a comparison between adults and children
Cortex
(1986)
Brain activation during dichotic presentations of consonant–vowel and musical instrument stimuli: a 15O-PET study
Neuropsychologia
The spatial and temporal signatures of word production components
Cognition
Functional asymmetry of the brain in dichotic listening
Cortex
From ear to brain
Brain Cogn.
Broca's area: nomenclature, anatomy, typology and asymmetry
Brain Lang.
The size of the anterior corpus callosum correlates with the strength of hemispheric encoding-retrieval asymmetry in the ventrolateral prefrontal cortex
Brain Res.
A forced-attention dichotic listening fMRI study on 113 subjects
Brain Lang.
A direct test for lateralization of language activation using fMRI: comparison with invasive assessments in children with epilepsy
Neuroimage
Attention-dependent changes of activation and connectivity in dichotic listening
Neuroimage
Valid conjunction inference with the minimum statistic
Neuroimage
Imaging the premotor areas
Curr. Opin. Neurobiol.
Reliability and validity of some handedness questionnaire items
Neuropsychologia
Processing of sub-syllabic speech units in the posterior temporal lobe: an fMRI study
Neuroimage
The functional neuroanatomy of prelexical processing in speech perception
Cognition
The planum temporale: a systematic, quantitative review of its structural, functional and clinical significance
Brain Res. Brain Res. Rev.
Meta-analysis of Go/No-go tasks demonstrating that fMRI activation associated with response inhibition is task-dependent
Neuropsychologia
Dichotic listening in man after section of neocortical commissures
Cortex
Extinction of auditory stimuli in hemineglect: space versus ear
Neuropsychologia
Activation of human auditory cortex during speech perception: effects of monaural, binaural, and dichotic presentation
Neuropsychologia
Hemispheric differences in hemodynamics elicited by auditory oddball stimuli
Neuroimage
Lateralization of auditory-cortex functions
Brain Res. Brain Res. Rev.
Dichotic listening reveals functional specificity in prefrontal cortex: an fMRI study
Neuroimage
Pre-SMA actively engages in conflict processing in human: a combined study of epicortical ERPs and direct cortical stimulation
Neuropsychologia
A new verbal reports fMRI dichotic listening paradigm for studies of hemispheric asymmetry
Neuroimage
What is right-hemisphere contribution to phonological, lexico-semantic, and sentence processing? Insights from a meta-analysis
Neuroimage
The corpus callosum in dichotic listening studies of hemispheric asymmetry: a review of clinical and experimental evidence
Neurosci. Biobehav. Rev.
The association of macro- and microstructure of the corpus callosum and language lateralisation
Brain Lang.
Identification of attention and cognitive control networks in a parametric auditory fMRI study
Neuropsychologia
Differential contributions of motor cortex, basal ganglia, and cerebellum to speech motor control: effects of syllable repetition rate evaluated by fMRI
Neuroimage
Functional significance of individual variations in callosal area
Neuropsychologia
Perceptual asymmetry on the dichotic fused words test and cerebral speech lateralization determined by the carotid sodium amytal test
Neuropsychologia
Models of hemispheric specialization
Psychol. Bull.
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