Gender Influences on Brain Responses to Errors and Post-Error Adjustments

Sexual dimorphisms have been observed in many species, including humans, and extend to the prevalence and presentation of important mental disorders associated with performance monitoring malfunctions. However, precisely which underlying differences between genders contribute to the alterations observed in psychiatric diseases is unknown. Here, we compare behavioural and neural correlates of cognitive control functions in 438 female and 436 male participants performing a flanker task while EEG was recorded. We found that males showed stronger performance-monitoring-related EEG amplitude modulations which were employed to predict subjects’ genders with ~72% accuracy. Females showed more post-error slowing, but both samples did not differ in regard to response-conflict processing and coupling between the error-related negativity (ERN) and consecutive behavioural slowing. Furthermore, we found that the ERN predicted consecutive behavioural slowing within subjects, whereas its overall amplitude did not correlate with post-error slowing across participants. These findings elucidate specific gender differences in essential neurocognitive functions with implications for clinical studies. They highlight that within- and between-subject associations for brain potentials cannot be interpreted in the same way. Specifically, despite higher general amplitudes in males, it appears that the dynamics of coupling between ERN and post-error slowing between men and women is comparable.

[1]  Boris Egloff,et al.  Gender differences in implicit and explicit anxiety measures , 2004 .

[2]  Alex R. Smith,et al.  Sex differences in the structural connectome of the human brain , 2013, Proceedings of the National Academy of Sciences.

[3]  M. Ullsperger,et al.  Post-Error Adjustments , 2011, Front. Psychology.

[4]  F. E. Grubbs Procedures for Detecting Outlying Observations in Samples , 1969 .

[5]  Daniel S. Margulies,et al.  Sex beyond the genitalia: The human brain mosaic , 2015, Proceedings of the National Academy of Sciences.

[6]  Pearl H Chiu,et al.  Neural evidence for enhanced error detection in major depressive disorder. , 2007, The American journal of psychiatry.

[7]  Tim P. Moran,et al.  Sex moderates the association between symptoms of anxiety, but not obsessive compulsive disorder, and error-monitoring brain activity: A meta-analytic review. , 2016, Psychophysiology.

[8]  Elena A. Allen,et al.  Acetylcholine Mediates Behavioral and Neural Post-Error Control , 2015, Current Biology.

[9]  Jan R. Wessel,et al.  Modulation of the error-related negativity by response conflict. , 2009, Psychophysiology.

[10]  Tom Eichele,et al.  Semi-automatic identification of independent components representing EEG artifact , 2009, Clinical Neurophysiology.

[11]  Adrian G. Fischer,et al.  Serotonin Reuptake Inhibitors and Serotonin Transporter Genotype Modulate Performance Monitoring Functions But Not Their Electrophysiological Correlates , 2015, The Journal of Neuroscience.

[12]  Sheng Zhang,et al.  Gender Differences in Cognitive Control: an Extended Investigation of the Stop Signal Task , 2009, Brain Imaging and Behavior.

[13]  P. Rabbitt Errors and error correction in choice-response tasks. , 1966, Journal of experimental psychology.

[14]  Avram J Holmes,et al.  Spatiotemporal dynamics of error processing dysfunctions in major depressive disorder. , 2008, Archives of general psychiatry.

[15]  Kenneth Kreutz-Delgado,et al.  AMICA : An Adaptive Mixture of Independent Component Analyzers with Shared Components , 2011 .

[16]  Francis S Collins,et al.  Policy: NIH to balance sex in cell and animal studies , 2014, Nature.

[17]  S. Tipper,et al.  Sex differences in eye gaze and symbolic cueing of attention , 2005, The Quarterly journal of experimental psychology. A, Human experimental psychology.

[18]  Peter E. Clayson,et al.  Making sense of all the conflict: a theoretical review and critique of conflict-related ERPs. , 2014, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[19]  Anders M. Dale,et al.  Sex-dependent association of common variants of microcephaly genes with brain structure , 2009, Proceedings of the National Academy of Sciences.

[20]  A. Engel,et al.  Trial-by-Trial Coupling of Concurrent Electroencephalogram and Functional Magnetic Resonance Imaging Identifies the Dynamics of Performance Monitoring , 2005, The Journal of Neuroscience.

[21]  L. Cahill,et al.  Sex Influences on the Brain: An Issue Whose Time Has Come , 2015, Neuron.

[22]  Markus Ullsperger,et al.  Real and Fictive Outcomes Are Processed Differently but Converge on a Common Adaptive Mechanism , 2013, Neuron.

[23]  Gijsbert Stoet,et al.  Sex differences in the processing of flankers , 2010, Quarterly journal of experimental psychology.

[24]  L. Cahill An issue whose time has come , 2017, Journal of neuroscience research.

[25]  Judith A. Hall,et al.  A Meta-analytic Review , 2002 .

[26]  F. Rijsdijk,et al.  Reaction time, inhibition, working memory and ‘delay aversion’ performance: genetic influences and their interpretation , 2006, Psychological Medicine.

[27]  C. Carter,et al.  Anterior cingulate cortex activity and impaired self-monitoring of performance in patients with schizophrenia: an event-related fMRI study. , 2001, The American journal of psychiatry.

[28]  Donald Laming,et al.  Information theory of choice-reaction times , 1968 .

[29]  Ilina Singh,et al.  Beyond polemics: science and ethics of ADHD , 2008, Nature Reviews Neuroscience.

[30]  M. Ullsperger,et al.  Specificity of performance monitoring changes in obsessive-compulsive disorder , 2014, Neuroscience & Biobehavioral Reviews.

[31]  C. Carter,et al.  The Timing of Action-Monitoring Processes in the Anterior Cingulate Cortex , 2002, Journal of Cognitive Neuroscience.

[32]  K. R. Ridderinkhof,et al.  The Role of the Medial Frontal Cortex in Cognitive Control , 2004, Science.

[33]  a.R.V.,et al.  Clinical neurophysiology , 1961, Neurology.

[34]  G. Hajcak,et al.  Electrocortical and behavioral measures of response monitoring in young children during a Go/No-Go task. , 2012, Developmental psychobiology.

[35]  Wim Fias,et al.  Post-error slowing: An orienting account , 2009, Cognition.

[36]  G. Hajcak,et al.  The error-related negativity (ERN) and psychopathology: toward an endophenotype. , 2008, Clinical psychology review.

[37]  M. Ullsperger,et al.  Neurophysiology of performance monitoring and adaptive behavior. , 2014, Physiological reviews.

[38]  Charles H Hillman,et al.  The relation of self-efficacy and error-related self-regulation. , 2011, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[39]  Raquel E Gur,et al.  Age group and sex differences in performance on a computerized neurocognitive battery in children age 8-21. , 2012, Neuropsychology.

[40]  Arnaud Delorme,et al.  EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis , 2004, Journal of Neuroscience Methods.

[41]  B. Silverstein Gender differences in the prevalence of somatic versus pure depression: a replication. , 2002, The American journal of psychiatry.

[42]  Tim P. Moran,et al.  On the relationship between anxiety and error monitoring: a meta-analysis and conceptual framework , 2013, Front. Hum. Neurosci..

[43]  Greg Hajcak,et al.  What We’ve Learned From Mistakes , 2012 .

[44]  M. Delgado-Rodríguez,et al.  Systematic review and meta-analysis. , 2017, Medicina intensiva.

[45]  S. Baron-Cohen The extreme male brain theory of autism , 2002, Trends in Cognitive Sciences.

[46]  Tom Eichele,et al.  Posterior Medial Frontal Cortex Activity Predicts Post-Error Adaptations in Task-Related Visual and Motor Areas , 2011, The Journal of Neuroscience.

[47]  S. Baron-Cohen,et al.  Neuroscience and Biobehavioral Reviews a Meta-analysis of Sex Differences in Human Brain Structure , 2022 .

[48]  Anna Weinberg,et al.  Integrating multiple perspectives on error-related brain activity: The ERN as a neural indicator of trait defensive reactivity , 2011, Motivation and Emotion.

[49]  N. Schor,et al.  The Essential Difference , 1996 .

[50]  Michael J. Larson,et al.  Sex differences in electrophysiological indices of conflict monitoring , 2011, Biological Psychology.

[51]  Adrian G. Fischer,et al.  Neural mechanisms and temporal dynamics of performance monitoring , 2014, Trends in Cognitive Sciences.

[52]  Andrew C Heath,et al.  Heritability of frontal brain function related to action monitoring. , 2008, Psychophysiology.

[53]  Anna Weinberg,et al.  Error-related brain activity in the age of RDoC: A review of the literature. , 2015, International Journal of Psychophysiology.

[54]  A. Preti,et al.  Gender and duration of untreated psychosis: a systematic review and meta‐analysis , 2012, Early intervention in psychiatry.

[55]  Birte U. Forstmann,et al.  How to measure post-error slowing: A confound and a simple solution , 2012 .

[56]  J. Becker,et al.  Sex differences in drug abuse , 2008, Frontiers in Neuroendocrinology.

[57]  Peter E Clayson,et al.  Sex differences in error-related performance monitoring , 2011, Neuroreport.

[58]  Tyrone D. Cannon,et al.  Women are more sensitive than men to prior trial events on the Stop-signal task. , 2014, British journal of psychology.

[59]  J. Cavanagh,et al.  Frontal midline theta reflects anxiety and cognitive control: Meta-analytic evidence , 2015, Journal of Physiology-Paris.

[60]  Wouter Hulstijn,et al.  Action monitoring in major depressive disorder with psychomotor retardation , 2008, Cortex.

[61]  I. Deary,et al.  Age and sex differences in reaction time in adulthood: results from the United Kingdom Health and Lifestyle Survey. , 2006, Psychology and aging.