Elsevier

Brain and Cognition

Volume 76, Issue 2, July 2011, Pages 300-309
Brain and Cognition

Smoking reduces language lateralization: A dichotic listening study with control participants and schizophrenia patients

https://doi.org/10.1016/j.bandc.2011.03.015Get rights and content

Abstract

Schizophrenia has been associated with deficits in functional brain lateralization. According to some authors, the reduction of asymmetry could even promote this psychosis. At the same time, schizophrenia is accompanied by a high prevalence of nicotine dependency compared to any other population. This association is very interesting, because sex-dependent effects of smoking in auditory language asymmetries have been reported recently, and the verbal domain is also one major focus in cognitive deficit studies of schizophrenia. Thus, the altered laterality pattern in schizophrenia could, at least in part, result from secondary artefacts due to smoking rather than being a pure cause of the disease itself. To test this hypothesis, the present study examined auditory language lateralization in 67 schizophrenia patients and in 72 healthy controls in a phonemic and an emotional dichotic listening task. Our findings replicate previous research, in that smoking reduces language lateralization in men in phonemic dichotic listening. In addition, we show that smoking also reduces laterality in women in the emotional dichotic listening task. Thus, smoking alters phonemic and emotional language asymmetries differentially for men and women, with a stronger effect for men in the left hemisphere phonemic task, and a stronger effect for women in the right hemisphere emotional task. Together, these findings point towards an effect of smoking which is possibly independent of sex and hemisphere. Importantly, by testing equal numbers of smoking and non-smoking patients and controls, we found no schizophrenia-associated asymmetry effect. Possible neurobiological mechanisms with which smoking may alter auditory microcircuits and thereby diminish left–right differences are discussed.

Highlights

► We examined language lateralization in schizophrenia and in control participants. ► No asymmetry-related difference between patients and control subjects was detected. ► Smoking reduces laterality index differentially for men and women. ► Men are affected in phonemic and women in emotional dichotic listening. ► Smoking may underlie controversies around altered lateralization in schizophrenia.

Introduction

Schizophrenia is a severe psychiatric disorder that affects about 1% of the population. Studies show that schizophrenia is associated with deficits of functional brain lateralization (Crow, 1997, Mitchell and Crow, 2005, Sommer et al., 2001). Sex differences and language deficits in the clinical symptomatology of schizophrenia are well established (reviewed in Flor-Henry, 1985, Wallentin, 2009); however, the neural mechanisms that produce these effects remain under debate. According to some authors (e.g., Crow, 2010) schizophrenia could even result from an altered asymmetry pattern.

Schizophrenia is also accompanied by an extremely high prevalence of nicotine dependency (Kumari and Postma, 2005, Ziedonis et al., 2008) and heavier smoking patterns (De Leon et al., 1995) compared to both the general population and other psychiatric disorders. Growing evidence points to neurobiological mechanisms underlying this significantly higher smoking prevalence. For example, converging evidence suggests that smoking modifies sensory gating deficits in schizophrenia, as well as increasing vigilance and attention (reviewed in Winterer, 2010). Based on several observations (e.g., Kumari & Postma, 2005), it has been proposed that smoking may be used as a self-medication by schizophrenic patients, because nicotine use has been found to transiently alleviate negative symptoms (Smith, Singh, Infante, Khandat, & Kloos, 2002) as well as cognitive impairments associated with the disorder (Adler et al., 1993, Depatie et al., 2002, Kumari et al., 2001, Levin et al., 1996, Olincy et al., 1998). These findings even extend to non-affected first-degree relatives of schizophrenia patients (Adler, Hoffer, Griffith, Waldo, & Freedman, 1992). Subsequent pharmacological challenge studies have further elucidated and characterized cognitive domains like attention and working memory targeted by nicotine consumption in schizophrenia (Harris et al., 2004, Sacco et al., 2005, Smith et al., 2006) and by nicotine exposure to non-smoking schizophrenia subjects (Barr et al., 2008), although challenge studies following smoking abstinence are likely confounded by withdrawal phenomena.

The confound of elevated smoking prevalence associated with its effects on cognition together with the notion of altered brain lateralization in schizophrenia is very interesting, because a recent study revealed sex-dependent effects of smoking in auditory language asymmetries (Hahn, Pogun, & Güntürkün, 2010). Using a consonant-vowel dichotic listening design in healthy adults, the authors showed that auditory language processing was adversely affected by smoking in men, which was accompanied by a decreased laterality index. In contrast, women remained unaffected by smoking. Further, a higher degree of lateralization was generally associated with a higher recognition rate on the dichotic listening task. Together, these findings argue for a greater vulnerability of the auditory system, and of auditory brain lateralization in particular, elicited by nicotine exposure in healthy male subjects. Notably, nicotine-mediated and sex-specific effects on laterality have been demonstrated in rats (Kanit, Koylu, Erdogan, & Pogun, 2005).

Sex differences have previously been observed in dichotic listening studies (Ikezawa et al., 2008, Meinschaefer et al., 1999, Wadnerkar et al., 2008), and fluctuations of sex hormones also elicit dynamic short-term changes in functional brain asymmetries (Bayer et al., 2008, Bibawi et al., 1995, Hausmann et al., 2002, Hausmann and Güntürkün, 2000, Heister et al., 1989, Mead and Hampson, 1996, Rode et al., 1995, Sanders and Wenmoth, 1998, Wadnerkar et al., 2008). Further differences between men and women also occur in various aspects of nicotine dependency and smoking habits (reviewed in Perkins et al., 2002, Pogun and Yararbas, 2009).

Importantly, the verbal domain, targeted by dichotic listening, is also one major focus of cognitive deficit studies of schizophrenia. In order to test the hypothesis that altered laterality might in fact result from secondary artefacts due to smoking rather than being a cause of the disease itself (Herzig, Tracy, Munafö, & Mohr, 2010), the present study examined auditory language lateralization of left and right hemisphere in smoking and non-smoking schizophrenic patients and healthy controls.

Section snippets

Participants

Seventy-two (36 female) healthy adults (mean age = 34.35 ± 12.62 years) recruited via newspaper advertisements served as controls. All control subjects were examined by a psychiatrist before testing; only those without a history of psychiatric axis I disorder according to DSM-IV (American Psychiatric Association, 1994) or substance abuse (other than nicotine dependency) were included in the study. Severe medical or neurological condition, any psychopharmacological treatment or first-degree family

Validity of dichotic listening tasks

The mean (±S.D.) laterality index of all 139 participants for phonemic dichotic listening was 41.86 (±43.80), indicating significant lateralization to the left speech dominant hemisphere (t(138) = 11.27; p < 0.001; 95% CI [34.51, 49.20]). More stimuli were correctly identified by the right ear (M = 69.48 (±21.74)) than by the left ear (M = 28.47 (±21.58); t(138) = 11.19; p < 0.001; Cohen’s d = 1.89), and stimuli perceived by the right ear (M = 1330.99 ms (±223.98)) were responded to faster than those detected by

Validity of tasks

This study employed two new dichotic listening tasks to examine sex-specific effects of smoking on left and right hemisphere language lateralization in schizophrenia patients and healthy controls. In this context, we created and validated new bi-syllabic stimuli, which elicit contrasting lateralization patterns based on the instruction to focus on phonemic or emotional information, respectively. In addition, reaction times were calculated. Monosyllabic consonant–vowel-consonant sounds are

Conclusion

We contribute two main findings. First, we show that smoking reduces functional language asymmetries. This is (possibly) independent of sex, and also of the language system under study: it applies in a similar way to a left hemispheric process of phonemic discrimination and a right hemispheric function of prosodic recognition. The mechanisms with which smoking alters auditory microcircuits and thereby diminishes left–right differences can presently only vaguely be inferred. The second main

Conflict of interest

None declared.

Acknowledgments

This research was supported by the DFG research Grant (Gu227/12) and by the DAAD PhD-Net Grant. For assistance with data collection, we would like to thank Miriam Biene and Jonas Lins, and we thank Osman Iyilikci for his help with task programming. The authors thank all participants of this study for contributing their time and effort. C.H. was supported by the International Graduate School of Neuroscience fellowship, the Ruhr-University Bochum Rectorate fund, and the “Studienstiftung des

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