Marco Hirnstein

Sex differences in language asymmetry are age-dependent and small: A large-scale, consonant–vowel dichotic listening study with behavioral and fMRI data

Men are often believed to have a functionally more asymmetrical brain organization than women, but the empirical evidence for sex differences in lateralization is unclear to date. Over the years we have collected data from a vast number of participants using the same consonant-vowel dichotic listening task, a reliable marker for language lateralization. One dataset comprised behavioral data from 1782 participants (885 females, 125 non-right-handers), who were divided in four age groups (children <10 yrs, adolescents = 10-15 yrs, younger adults = 16-49 yrs, and older adults >50 yrs). In addition, we had behavioral and functional imaging (fMRI) data from another 104 younger adults (49 females, aged 18-45 yrs), who completed the same dichotic listening task in a 3T scanner. This database allowed us to comprehensively test whether there is a sex difference in functional language lateralization. Across all participants and in both datasets a right ear advantage (REA) emerged, reflecting left-hemispheric language lateralization. Accordingly, the fMRI data revealed a leftward asymmetry in superior temporal lobe language processing areas. In the N = 1782 dataset no main effect of sex but a significant sex by age interaction emerged: the REA increased with age in both sexes but as a result of an earlier onset in females the REA was stronger in female than male adolescents. In turn, male younger adults showed greater asymmetry than female younger adults (accounting for <1% of variance). There were no sex differences in children and older adults. The males in the fMRI dataset (N = 104) also had a greater REA than females (accounting for 4% of variance), but no sex difference emerged in the neuroimaging data. Handedness did not affect these findings. Taken together, our findings suggest that sex differences in language lateralization as assessed with dichotic listening exist, but they are (a) not necessarily reflected in fMRI data, (b) age-dependent and (c) relatively small.

Auditory hallucinations and reduced language lateralization in schizophrenia: a meta-analysis of dichotic listening studies.

Reduced left-hemispheric language lateralization has been proposed to be a trait marker for schizophrenia, but the empirical evidence is ambiguous. Recent studies suggest that auditory hallucinations are critical for whether a patient shows reduced language lateralization. Therefore, the aim of the study was to statistically integrate studies investigating language lateralization in schizophrenia patients using dichotic listening. To this end, two meta-analyses were conducted, one comparing schizophrenia patients with healthy controls (n = 1407), the other comparing schizophrenia patients experiencing auditory hallucinations with non-hallucinating controls (n = 407). Schizophrenia patients showed weaker language lateralization than healthy controls but the effect size was small (g = -0.26). When patients with auditory hallucinations were compared to non-hallucinating controls, the effect size was substantially larger (g = -0.45). These effect sizes suggest that reduced language lateralization is a weak trait marker for schizophrenia as such and a strong trait marker for the experience of auditory hallucinations within the schizophrenia population.

Disentangling the relationship between hemispheric asymmetry and cognitive performance

It is widely believed that advantages of hemispheric asymmetries originated in better cognitive processing, hence it is often implied that the relationship between hemispheric asymmetry and cognitive performance is linearly positive: the higher the degree of lateralization in a specific cognitive domain, the better the performance in a corresponding task. Yet, the empirical evidence for this notion is mixed and the statistical methods to analyze this relationship have been criticized. The present study therefore investigated the relationship between hemispheric asymmetries and cognitive performance in two behavioral tasks (a left-lateralized word-matching task and a right-lateralized face-decision task) in 230 participants (140 women, 90 men) by using two different approaches. Both methods correspondingly revealed that a relationship between hemispheric asymmetries and cognitive performance does exist. Contrary to a positive (linear) relationship however, the data could be best described by an inverted U-shaped curve. Although the optimal degree of lateralization seemed to be task-specific, a slight or moderate degree of hemispheric asymmetry achieved best cognitive performance in all tasks. Moreover, performances deteriorated towards extreme ends of lateralization (i.e., participants with either extreme left or right hemispheric biases). Taken together, the present study provides evidence against the notion that higher lateralization is related to enhanced cognitive performance.

The evolutionary origins of functional cerebral asymmetries in humans: Does lateralization enhance parallel processing?

Functional cerebral asymmetries (FCAs) are a fundamental principle of brain organization in many species. However, little is known about why they have evolved. Since FCAs are such a widespread phenomenon they seem to constitute an evolutionary selective advantage. According to a prominent hypothesis, an asymmetric brain should be associated with advantages in parallel processing, i.e. doing two tasks simultaneously. The strong version of this hypothesis implies that lateralized, instantaneous and complementary tasks are performed more efficiently with a highly lateralized brain. Using a visual half-field procedure, we wanted to test this strong version of the parallel-processing hypothesis in humans. Thirty-two participants (17 women, 15 men) were investigated. First, we assessed the degree of lateralization in a face/non-face and a word/non-word discrimination task favouring the right and left hemisphere, respectively. Based on a median split, subjects were divided into a rather symmetric and a rather asymmetric group. Then, all participants completed both tasks simultaneously. The results revealed that the rather symmetrically organized participants outperformed asymmetric participants in accuracy and response times. Hence, the strong version of the parallel-processing hypothesis has to be revised.

Excess of non-right-handedness in schizophrenia: meta-analysis of gender effects and potential biases in handedness assessment

BACKGROUND The notion that schizophrenia is characterised by increased non-right-handedness is a cornerstone of the theory that schizophrenia arises from, and is genetically linked to, abnormal brain lateralisation. Reviews and meta-analyses have reported higher rates of non-right-handers in patients with schizophrenia. However, this was suggested to be the result of a gender artefact or a hidden bias in self-report handedness questionnaires. AIMS To investigate using a meta-analytical approach whether the excess of non-right-handedness is seen in both females and males, and also when handedness is assessed behaviourally. METHOD Electronic databases were searched for studies that reported (a) the rate of female and male non-right-handers in schizophrenia compared with controls and (b) the rate of non-right-handers in schizophrenia (regardless of gender) based on behavioural handedness assessment. RESULTS The odds ratios (ORs) for females (OR = 1.63; based on 621 patients, 3747 controls) and males (OR = 1.50; based on 1213 patients, 3800 controls) differed significantly from 1.0, indicating both female and male patients were more often non-right-handed than controls. Moreover, there was an excess of non-right-handedness in patients with schizophrenia when handedness was assessed behaviourally: OR = 1.84 (1255 patients, 6260 controls). Even when both gender and behavioural handedness assessment were controlled for simultaneously, the excess of non-right-handedness persisted. CONCLUSIONS The findings clearly demonstrate that the excess of non-right-handedness in schizophrenia does not result from a gender artefact or from biased handedness questionnaires. It is a true empirical effect and may indeed reflect a genetic link between schizophrenia and brain lateralisation.

Auditory space perception in left- and right-handers.

Several studies have shown that handedness has an impact on visual spatial abilities. Here we investigated the effect of laterality on auditory space perception. Participants (33 right-handers, 20 left-handers) completed two tasks of sound localization. In a dark, anechoic, and sound-proof room, sound stimuli (broadband noise) were presented via 21 loudspeakers mounted horizontally (from 80 degrees on the left to 80 degrees on the right). Participants had to localize the target either by using a swivel hand-pointer or by head-pointing. Individual lateral preferences of eye, ear, hand, and foot were obtained using a questionnaire. With both pointing methods, participants showed a bias in sound localization that was to the side contralateral to the preferred hand, an effect that was unrelated to their overall precision. This partially parallels findings in the visual modality as left-handers typically have a more rightward bias in visual line bisection compared with right-handers. Despite the differences in neural processing of auditory and visual spatial information these findings show similar effects of lateral preference on auditory and visual spatial perception. This suggests that supramodal neural processes are involved in the mechanisms generating laterality in space perception.

How brain asymmetry relates to performance – a large-scale dichotic listening study

All major mental functions including language, spatial and emotional processing are lateralized but how strongly and to which hemisphere is subject to inter- and intraindividual variation. Relatively little, however, is known about how the degree and direction of lateralization affect how well the functions are carried out, i.e., how lateralization and task performance are related. The present study therefore examined the relationship between lateralization and performance in a dichotic listening task for which we had data available from 1839 participants. In this task, consonant-vowel syllables are presented simultaneously to the left and right ear, such that each ear receives a different syllable. When asked which of the two they heard best, participants typically report more syllables from the right ear, which is a marker of left-hemispheric speech dominance. We calculated the degree of lateralization (based on the difference between correct left and right ear reports) and correlated it with overall response accuracy (left plus right ear reports). In addition, we used reference models to control for statistical interdependency between left and right ear reports. The results revealed a u-shaped relationship between degree of lateralization and overall accuracy: the stronger the left or right ear advantage, the better the overall accuracy. This u-shaped asymmetry-performance relationship consistently emerged in males, females, right-/non-right-handers, and different age groups. Taken together, the present study demonstrates that performance on lateralized language functions depends on how strongly these functions are lateralized. The present study further stresses the importance of controlling for statistical interdependency when examining asymmetry-performance relationships in general.

Sex differences in left–right confusion depend on hemispheric asymmetry

Numerous studies have reported that women believe they are more susceptible to left-right confusion than men. Indeed, some studies have also found sex differences in behavioural tasks. It has been suggested that women have more difficulties with left-right discrimination, because they are less lateralised than men and a lower degree of lateralisation might lead to more left-right confusion (LRC). However, those studies reporting more left-right confusion for women have been criticised because the tasks that have been used involved mental rotation, a spatial ability in which men typically excel. In the present study, 34 right-handed women and 31 right-handed men completed two behavioural left-right discrimination tasks, in which mental rotation was either experimentally controlled for or was not needed. To measure the degree of hemispheric asymmetry participants also completed a dichotic listening test. Although women were not less lateralised than men, both tasks consistently revealed that women were more susceptible to left-right confusion than men. However, only women with a significant right ear advantage in the dichotic listening test had more difficulties in LRC tasks than men. There was no sex difference in less lateralised participants. This finding suggests that the impact of functional verbal asymmetries on LRC is mediated by sex.

Functional cerebral asymmetry in auditory motion perception.

Several studies have shown a right-hemispheric advantage for sound localisation. However, most of these studies used stationary sound stimuli, although in most everyday situations humans are in motion when localising sound, or face a moving sound source. To elucidate the question of a functional asymmetry in cortical processing of auditory motion information, we tested 23 neurologically healthy human participants. Virtual leftward or rightward motion (broadband noise) was presented with variable movement angles (MA) in the horizontal plane (via headphones) in either the participants’ left or right hemispace. Participants had to indicate whether the sound moved left or rightward. The frequency of “right” judgements determined as a function of MA had a sigmoidal shape in both hemispaces, indicating significant overall discrimination of motion direction. However, the frequency of correct judgements revealed a significantly better performance for the left than for the right hemispace, suggesting a superiority of the right hemisphere. This finding is in agreement with recent neuroimaging results showing higher right-hemispheric activity during localisation of moving sounds. The results might also point to a supramodal right-hemisphere advantage in the attentional processing of motion perception.

Emotional prosody modulates attention in schizophrenia patients with hallucinations

Recent findings have demonstrated that emotional prosody (EP) attracts attention involuntarily (Grandjean et al., 2008). The automat shift of attention toward emotionally salient stimuli can be overcome by attentional control (Hahn et al., 2010). Attentional control is impaired in schizophrenia, especially in schizophrenic patients with hallucinations because the “voices” capture attention increasing the processing load and competing for top-down resources. The present study investigates how involuntary attention is driven by implicit EP in schizophrenia with auditory verbal hallucinations (AVH) and without (NAVH). Fifteen AVH patients, 12 NAVH patients and 16 healthy controls (HC) completed a dual-task dichotic listening paradigm, in which an emotional vocal outburst was paired with a neutral vocalization spoken in male and female voices. Participants were asked to report the speakers gender while attending to either the left or right ear. NAVH patients and HC revealed shorter response times for stimuli presented to the attended left ear than the attended right ear. This laterality effect was not present in AVH patients. In addition, NAVH patients and HC showed faster responses when the EP stimulus was presented to the unattended ear, probably because of less interference between the attention-controlled gender voice identification task and involuntary EP processing. AVH patients did not benefit from presenting emotional stimuli to the unattended ear. The findings suggest that similar to HC, NAVH patients show a right hemispheric bias for EP processing. AVH patients seem to be less lateralized for EP and therefore might be more susceptible to interfering involuntary EP processing; regardless which ear/hemisphere receives the bottom up input.