Normal Sexual Dimorphism in Theory of Mind Circuitry is Reversed in Schizophrenia

Overview

Journal Soc Neurosci

Publisher Routledge

Date 2018 Oct 31

PMID 30373474

Citations 2

Authors

Julie Walsh-Messinger

Christine Stepanek

Julia Wiedemann

Deborah Goetz

Raymond R Goetz

Dolores Malaspina

Affiliations

Soon will be listed here.

Abstract

The ability to mentalize, or theory of mind (ToM), is sexually dimorphic in humans and impaired in schizophrenia. This sex-stratified study probed cognitive (indexed by intelligence) and affective (indexed by olfactory tasks) contributions to ToM performance in 37 individuals with schizophrenia and 31 healthy controls. The schizophrenia group showed impairments in mental state identification and inferring intentions compared to controls. Higher intelligence was correlated with mental state identification and inferring intentions in healthy females, whereas better smell identification was associated with mental state identification in healthy males. Conversely, higher intelligence was associated with mental state identification and inferring intentions in schizophrenia males, while better smell identification was correlated with mental state identification in schizophrenia females. These findings suggest that for ToM circuitry, the cognitive influences in healthy females and affective influences in healthy males are reversed in schizophrenia and may be displaced to lower circuitries by disease pathology. Symptom associations with emotion and cognition are also dimorphic, plausibly due to similar pathology superimposed on normal sex-specific circuitries. Males appear to rely on limbic processing for ToM, and disruption to this circuitry may contribute to development of negative symptoms. These findings highlight the importance of utilizing sex-stratified designs in schizophrenia research.

Citing Articles

Sex Differences in Cognition in Schizophrenia: What We Know and What We Do Not Know.

Freeman H, Lee J Curr Top Behav Neurosci. 2022; 63:463-474.

PMID: 36271194 DOI: 10.1007/7854_2022_394.

Sex Differences in Social Cognition and Association of Social Cognition and Neurocognition in Early Course Schizophrenia.

Kubota R, Okubo R, Ikezawa S, Matsui M, Adachi L, Wada A Front Psychol. 2022; 13:867468.

PMID: 35496257 PMC: 9051335. DOI: 10.3389/fpsyg.2022.867468.

References

Saltzman J, Strauss E, Hunter M, Archibald S . Theory of mind and executive functions in normal human aging and Parkinson's disease. J Int Neuropsychol Soc. 2000; 6(7):781-8. DOI: 10.1017/s1355617700677056. View

Potter H, Butters N . An assessment of olfactory deficits in patients with damage to prefrontal cortex. Neuropsychologia. 1980; 18(6):621-8. DOI: 10.1016/0028-3932(80)90101-3. View

Corcoran R, Mercer G, Frith C . Schizophrenia, symptomatology and social inference: investigating "theory of mind" in people with schizophrenia. Schizophr Res. 1995; 17(1):5-13. DOI: 10.1016/0920-9964(95)00024-g. View

Martin A, Dzafic I, Robinson G, Reutens D, Mowry B . Mentalizing in schizophrenia: A multivariate functional MRI study. Neuropsychologia. 2016; 93(Pt A):158-166. DOI: 10.1016/j.neuropsychologia.2016.10.013. View

Mimura M, Oeda R, Kawamura M . Impaired decision-making in Parkinson's disease. Parkinsonism Relat Disord. 2006; 12(3):169-75. DOI: 10.1016/j.parkreldis.2005.12.003. View

Bliksted V, Fagerlund B, Weed E, Frith C, Videbech P . Social cognition and neurocognitive deficits in first-episode schizophrenia. Schizophr Res. 2014; 153(1-3):9-17. DOI: 10.1016/j.schres.2014.01.010. View

Boesveldt S, Yee J, McClintock M, Lundstrom J . Olfactory function and the social lives of older adults: a matter of sex. Sci Rep. 2017; 7:45118. PMC: 5361152. DOI: 10.1038/srep45118. View

Stockhorst U, Pietrowsky R . Olfactory perception, communication, and the nose-to-brain pathway. Physiol Behav. 2004; 83(1):3-11. DOI: 10.1016/j.physbeh.2004.07.018. View

Bora E, Yucel M, Pantelis C . Theory of mind impairment in schizophrenia: meta-analysis. Schizophr Res. 2009; 109(1-3):1-9. DOI: 10.1016/j.schres.2008.12.020. View

10.

Stone V, Baron-Cohen S, Calder A, Keane J, Young A . Acquired theory of mind impairments in individuals with bilateral amygdala lesions. Neuropsychologia. 2002; 41(2):209-20. DOI: 10.1016/s0028-3932(02)00151-3. View

11.

Brune M . "Theory of mind" in schizophrenia: a review of the literature. Schizophr Bull. 2005; 31(1):21-42. DOI: 10.1093/schbul/sbi002. View

12.

Andreasen N, Flaum M, Swayze 2nd V, Tyrrell G, Arndt S . Positive and negative symptoms in schizophrenia. A critical reappraisal. Arch Gen Psychiatry. 1990; 47(7):615-21. DOI: 10.1001/archpsyc.1990.01810190015002. View

13.

Seidman L, Goldstein J, Goodman J, Koren D, Turner W, Faraone S . Sex differences in olfactory identification and Wisconsin Card Sorting performance in schizophrenia: relationship to attention and verbal ability. Biol Psychiatry. 1997; 42(2):104-15. DOI: 10.1016/S0006-3223(96)00300-9. View

14.

Harrington L, Langdon R, Siegert R, McClure J . Schizophrenia, theory of mind, and persecutory delusions. Cogn Neuropsychiatry. 2006; 10(2):87-104. DOI: 10.1080/13546800344000327. View

15.

Eslinger P, Damasio A, Van Hoesen G . Olfactory dysfunction in man: anatomical and behavioral aspects. Brain Cogn. 1982; 1(3):259-85. DOI: 10.1016/0278-2626(82)90028-8. View

16.

Malaspina D, Keller A, Antonius D, Messinger J, Goetz D, Harkavy-Friedman J . Olfaction and cognition in schizophrenia: sex matters. J Neuropsychiatry Clin Neurosci. 2012; 24(2):165-75. DOI: 10.1176/appi.neuropsych.11070154. View

17.

McGlashan T, Bardenstein K . Gender differences in affective, schizoaffective, and schizophrenic disorders. Schizophr Bull. 1990; 16(2):319-29. DOI: 10.1093/schbul/16.2.319. View

18.

Frank C, Baron-Cohen S, Ganzel B . Sex differences in the neural basis of false-belief and pragmatic language comprehension. Neuroimage. 2014; 105:300-11. DOI: 10.1016/j.neuroimage.2014.09.041. View

19.

Strauss G, Keller W, Koenig J, Sullivan S, Gold J, Buchanan R . Endogenous oxytocin levels are associated with the perception of emotion in dynamic body expressions in schizophrenia. Schizophr Res. 2015; 162(1-3):52-6. PMC: 4339450. DOI: 10.1016/j.schres.2015.01.022. View

20.

De Achaval D, Costanzo E, Villarreal M, Jauregui I, Chiodi A, Castro M . Emotion processing and theory of mind in schizophrenia patients and their unaffected first-degree relatives. Neuropsychologia. 2009; 48(5):1209-15. DOI: 10.1016/j.neuropsychologia.2009.12.019. View