Elsevier

NeuroImage

Volume 55, Issue 3, 1 April 2011, Pages 1393-1400
NeuroImage

Neural correlates of reality monitoring during adolescence

https://doi.org/10.1016/j.neuroimage.2010.12.058Get rights and content

Abstract

Background

Reality monitoring processes serve the critical function of discriminating between externally derived information and self-generated information. Several reality monitoring studies with healthy adult participants have identified the anterior prefrontal cortex (PFC) as consistently engaged during the recollection of self-generated contextual cues. Furthermore, reduced activity of medial PFC has been linked with schizotypal trait expression of delusion and hallucination-like symptoms in healthy adults undergoing fMRI reality-monitoring tasks. The present study seeks to examine the cerebral underpinnings of reality monitoring during adolescence, a developmental stage where the expression of schizotypal traits may increase risk for psychosis.

Method

A group of 33 adolescents, assessed using the Schizotypal Personality Scale (SPQ), underwent fMRI while performing a reality monitoring task. After an encoding session where the subject or the experimenter read out a series of complete or incomplete word pairs, subjects were presented with the first word of studied word pairs and asked whether the corresponding word had been: (1) perceived or produced (context monitoring), or (2) read by the subject or by the experimenter (origin monitoring).

Results

Analyses revealed a common set of activated brain areas during both context and origin monitoring conditions. When compared to context monitoring, origin monitoring was associated with greater activation in anterior PFC within Brodmann area 10 (BA 10). Correlation analyses revealed that reduced signal change in BA 10 during origin monitoring was associated with greater schizotypal trait expression.

Conclusion

Much like adults performing a similar reality monitoring task, adolescents exhibit a common pattern of brain activity during origin and context monitoring, with functional specialization within the prefrontal cortex involving preferential activation of BA 10 during origin monitoring. Greater schizotypal trait expression appears to be significantly associated to reduced BA 10 activity during origin monitoring trials. Results are discussed in relation to cortical specialization within the PFC and trait expression during adolescence.

Research Highlights

► Adolescent context and origin monitoring recruit similar cerebral activation. ► Origin monitoring selectively recruits increased BA 10 activity. ► BA 10 activity during origin monitoring correlates with adolescent schizotypy.

Introduction

Reality monitoring processes allow us to discriminate between perceptually based and reflectively based mental events (Johnson and Raye, 1981). Employing the term reality here commonly alludes to an event's external, perceptually grounded source. When distinguishing a past perception from a past reflection, we effectively consider the available contextual information (modalities, features, etc.). This process naturally contrasts with considering information of reflective nature, such as thoughts and associated cognitive processes that more readily indicate an event's internal source (Johnson et al., 1993). Discriminating between perceptually and reflectively based information may be facilitated by self-relevant cues (Foley et al., 1983). In other words, one may more promptly identify an event's perceptual or reflective source when information on the event's origin (who delivered the information) is available to the individual (Johnson and Raye, 1981). Together, perceptual/reflective monitoring (hereby described as context monitoring) and self/other monitoring (hereby described as origin information) thus constitute two essential components of efficient reality monitoring.

Current neuroimaging literature supports the notion that different reality monitoring processes share neural underpinnings (Simons et al., 2006a). Evidence for this is brought by functional neuroimaging studies consistently reporting overlapping brain activity during origin and context monitoring tasks, in cerebral areas that include the lateral prefrontal cortices (PFC), the anterior cingulate, the insula, and the lateral parietal cortices (Simons et al., 2008). However these same studies also highlight subtle yet critical differences in neural activation between the two monitoring processes, showing that origin monitoring engages significantly more activity in the rostral prefrontal cortex within Brodmann area 10 (BA 10) compared to cerebral activity sustained during context monitoring (Simons et al., 2006a, Simons et al., 2005, Simons et al., 2008).

A recent conceptualization of BA 10 activity modulation argues for its implication in the coordination of stimulus-dependent and stimulus-independent mental activity (Burgess et al., 2007). Specifically, this part of the anterior prefrontal cortex is thought to act as a gateway regulating the processing of perceptually or reflectively based information. Several studies lend support to the gateway hypothesis (Gilbert et al., 2005, Simons et al., 2006b), and more specifically, to the implication of BA 10 in reality monitoring tasks that require the participant to distinguish between externally or internally derived information (Gilbert et al., 2010, Gilbert et al., 2006). Moreover, because stimulus-independent thought most likely originates from one's self, we may expect that BA 10 play a critical role in disentangling mental content originating from the self from that originating from another agent.

Interestingly, Simons et al. (2008) recently observed that schizotypal personality trait expression, which is characterized by proneness to experience delusion and hallucination-like phenomena, is associated with reduced BA 10 activity in healthy participants performing an origin monitoring task. Both context and origin monitoring are particularly relevant to schizotypal trait expression, as they usually involve a confusion between the perceptual and reflective nature of mental events (such as command hallucinations), a misattribution of self and other origin (such as experiencing alien thought control), or a combination of both (such as hearing voices outside one's head). The data reported by Simons et al. (2008) may suggest that reduced BA 10 activity during origin monitoring could, in part, reveal a faulty gateway function increasing the propensity to experience schizotypal cognitions.

Because schizotypal trait expression constitutes the single most predictive factor for the development of schizophreniform disorders during adulthood (Miller et al., 2002, Poulton et al., 2000), examining the neural underpinnings of reality monitoring during adolescence could provide critical information on the developmental pathways leading to minor or clinically relevant manifestations of schizotypy (Bentall et al., 2007). Several theorists already argue for an association between reality monitoring deficits and the expression of psychosis (Bentall et al., 1991, Frith, 1992), and numerous reports observe reality monitoring deficits in schizophrenic patients (Keefe et al., 2002, Vinogradov et al., 1997), healthy adults exhibiting schizotypal manifestations (Larøi et al., 2005, Larøi et al., 2004), but also in diverse groups of adolescents who report increased schizotypal trait expression (Debbané et al., 2009a, Debbané et al., 2009b). To date however, the neural underpinnings of reality monitoring processes during adolescence remain unknown. This question entails further relevance in light of the important cortical maturation taking place during adolescence (Casey et al., 2008), most notably in the medial frontal cortices (Shaw et al., 2008). Considering that psychotic psychopathology most commonly declares itself during the early years of adulthood, it appears crucial to examine the cognitive and neural underpinnings that may mediate schizotypal trait expression early on during adolescence.

The present fMRI study examines context and origin monitoring in a sample of adolescents representative of the wide range of schizotypal trait expression. The objectives are threefold: 1) To examine the neural underpinnings of reality monitoring during adolescence; 2) To examine the potential overlapping and segregated neural activations between context and origin monitoring during adolescence; and 3) To characterize the association between schizotypal trait expression and reality monitoring processes during adolescence. On the basis of previous studies with adult participants, we first expect to find overlapping cortical activation for context and origin monitoring in our sample. Second, we hypothesize that medial anterior PFC within BA 10 will yield significantly more activation during origin monitoring trials when compared to context monitoring trials. Finally, we predict that schizotypal trait expression scores will be associated with BA 10 activation during origin monitoring trials.

Section snippets

Participants

Thirty-three right handed teenagers (18 females) with a mean age of 16.61 years (s.d. = 1.9), with normal or corrected to normal vision volunteered for participation. Participants were recruited by word of mouth from secondary schools in the state of Geneva (n = 17), and also through a participant pool collected between 2006 and 2008 in the child and adolescent outpatient public service, the Office Médico-Pédagogique (n = 16) (Debbané et al., 2009a). At time of testing, none of the participants were

Behavioural results

Participants' performance for context and origin trials are reported in Table 1. Comparisons related to condition performances revealed significantly superior retrieval performances in the origin condition compared to the context condition (t(32) = −6.12, p < 0.001). Within the origin condition, we observed a significant difference in favour of experimenter trials (t(32) = 6.54, p < 0.001) in comparison to self trials. In the context condition, we observed significant difference in favour of

Discussion

Results from the fMRI reality monitoring paradigm administered to a sample of adolescents provide support to the hypotheses tested in this study. First, we observed that different reality monitoring processes, namely origin and context monitoring, largely share underlying neural activation patterns including the anterior prefrontal cortex (PFC), the dorsolateral PFC, the MTG, the posterior cingulate gyrus and both medial and lateral regions in the parietal cortex. Second, we observed that

Acknowledgments

The authors would like to thank the volunteer participants, as well as Drs Dario Balanzin and Serges Djapo-Yogwa for their collaboration. Additional thanks go to the CIBM/LAVIM neuroimaging platform, especially to François Lazeyras, Pascal Challande and Frank Henry. We would also like to acknowledge Michal Epstein and Deborah Badoud for their contributions to data collection. This work was funded by the Gertrude Von Meissner Foundation (ME 7871) grant to S. Eliez and M. Debbané, and by the

References (37)

  • B.J. Casey et al.

    The adolescent brain

    Ann. NY Acad. Sci.

    (2008)
  • C.A. Cocosco et al.

    Brainweb: online interface to a 3D mri simulated brain database

    Neuroimage

    (1997)
  • M. Debbané et al.

    Cognitive and emotional associations to positive schizotypy during adolescence

    J. Child Psychol. Psychiatry

    (2009)
  • M. Debbané et al.

    Monitoring of self-generated speech in adolescents with 22q11.2 deletion syndrome

    Br. J. Clin. Psychol.

    (2009)
  • P. Dumas et al.

    validation of the french version of the raine schizotypal personality disorder questionnaire—categorial and dimensional approach to schizotypal personality traits in a normal student population

    Encephale

    (2000)
  • S. Escher

    Determinants of outcome in the pathways through care for children hearing voices

    Int. J. Soc. Welf.

    (2004)
  • S. Escher et al.

    Independent course of childhood auditory hallucinations: a sequential 3-year follow-up study

    Br. J. Psychiatry Suppl.

    (2002)
  • M.A. Foley et al.

    Age-related changes in confusion between memories for thoughts and memories for speech

    Child Dev.

    (1983)
  • Cited by (0)

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