Demystifying cognitive flexibility: Implications for clinical and developmental neuroscience

doi:10.1016/j.tins.2015.07.003

Trends in Neurosciences

Volume 38, Issue 9, September 2015, Pages 571-578

https://doi.org/10.1016/j.tins.2015.07.003 Get rights and content

Highlights

•
Cognitive flexibility is essential for appropriate behavioral responses.
•
Neural correlates of cognitive flexibility include systems for executive control.
•
Cognitive flexibility undergoes protracted development and is impaired in disorders.
•
Neural flexibility and brain dynamics may underlie cognitive flexibility.

Cognitive flexibility, the readiness with which one can selectively switch between mental processes to generate appropriate behavioral responses, develops in a protracted manner and is compromised in several prevalent neurodevelopmental disorders. It is unclear whether cognitive flexibility arises from neural substrates distinct from the executive control network (ECN) or from the interplay of nodes within this and other networks. Here we review neuroimaging studies of cognitive flexibility, focusing on set shifting and task switching. We propose that more consistent operationalization and study of cognitive flexibility is required in clinical and developmental neuroscience. We suggest that an important avenue for future research is the characterization of the relationship between neural flexibility and cognitive flexibility in typical and atypical development.

Section snippets

Significance of cognitive flexibility

Cognitive flexibility is the ability to appropriately adjust one's behavior according to a changing environment 1, 2 (see Glossary). Cognitive flexibility enables an individual to work efficiently to disengage from a previous task, reconfigure a new response set, and implement this new response set to the task at hand. Greater cognitive flexibility is associated with favorable outcomes throughout the lifespan, such as better reading abilities in childhood [3], higher resilience to negative life

Defining and measuring cognitive flexibility

Cognitive flexibility can be particularly difficult to examine due to the multitude of ways it has been described in the literature. In some instances cognitive flexibility is discussed in the context of processes requiring shifts in attention (e.g., attentional flexibility [7], attention switching [8], attentional set shifting [9]). In others, it is operationalized by the tasks that are used to measure it (e.g., set shifting [10], task switching [11]).

Here we aim to more precisely define

EFs required for cognitive flexibility

Several subdomains of EF act coherently to successfully implement cognitive flexibility (Figure 1). In constantly changing environments, individuals must first identify how their surroundings have changed by directing attention to those elements that are in flux. After ascertaining that a previous strategy is not appropriate in the new environment, individuals must inhibit previous responses and reconfigure a new strategy. Individuals take in information and manipulate it in real time to

Brain networks underlying cognitive flexibility

Recent meta-analyses of neuroimaging studies of cognitive flexibility in neurotypical adults have identified a distributed network of frontoparietal regions involved in flexible switching, including high-level cortical association areas (vlPFC, dlPFC, anterior cingulate, right AI), the premotor cortex, the inferior and superior parietal cortices, the inferior temporal cortex, the occipital cortex, and subcortical structures such as the caudate and thalamus 26, 27. Ongoing work is attempting to

Delineating a cognitive flexibility network in the context of an ECN

Cognition is achieved through the interplay of anatomically separated and interconnected local networks defining large-scale networks subserving attention, language, memory, and other cognitive processes [38]. Network views of cognition and behavior currently dominate the cognitive neuroscience landscape 39, 40. Cognitive flexibility is likely to emerge from the interplay of specific nodes in the frontal and parietal cortices, all of which are necessary while each provides a relatively specific

Behavioral trajectories

Cognitive flexibility skills begin to develop in early childhood, with a sharp increase in abilities between 7 and 9 years of age. Cognitive flexibility becomes largely mature by 10 years of age [43] but skills continue to improve throughout adolescence and into adulthood 44, 45, reaching their peak between the ages of 21 and 30 years [46]. Components of EF involved in cognitive flexibility follow different developmental trajectories (Figure 3). Inhibition develops as early as 12 months and is

Executive dysfunction and cognitive inflexibility

The rudimentary versions of EF that emerge in infancy lay a foundation for the emergence of more mature EFs that underlie self-control. In middle childhood, executive dysfunction that was previously masked may become apparent as children begin to be challenged academically and socially [45]. In particular, decreased levels of cognitive flexibility and working memory are associated with a range of academic deficits from reading to science [3]. In adolescence, intact EF is demonstrated as the

Future directions: relating neural flexibility and brain dynamics to cognitive flexibility

An emerging literature suggests that brain signal variability, or neural variability, may represent a complex neural system capable of great dynamic range and an enhanced ability to efficiently process varied unexpected external stimuli [74]. Brains of older individuals exhibiting less consistent behavioral performance exhibit reduced variability of blood-oxygen level-dependent (BOLD) signal compared with brains of younger individuals [75]. These findings have led to the proposal that

Concluding remarks

Cognitive flexibility is a critical skill that enables individuals to accurately and efficiently respond in the face of changing environments. The specific interactions among key network nodes that are required to successfully implement cognitive flexibility continue to be characterized (Box 2). Important considerations need to be accounted for as researchers begin to examine the development of cognitive flexibility and its disruption in various disorders such as ASD. Taking into account

Acknowledgments

This work was supported by awards K01MH092288 and R01MH107549 from the National Institute of Mental Health, a Slifka/Ritvo Innovation in Autism Research Award, and a NARSAD Young Investigator Grant to L.Q.U.

Glossary

Autism spectrum disorder (ASD): a neurodevelopmental disorder characterized by core deficits in social interaction/communication and the presence of RRBs; those with ASD also have impaired cognitive flexibility 65, 69, 71, 72.
Cognitive flexibility: an emergent property of efficient EF; the ability to appropriately and efficiently adjust one's behavior according to a changing environment 1, 2, most commonly measured with task switching and set shifting tasks.
Dynamic functional connectivity: functional

References (89)

Q. Chen
Association of creative achievement with cognitive flexibility by a combined voxel-based morphometry and resting-state functional connectivity study
Neuroimage
(2014)
A.M. Owen
Extra-dimensional versus intra-dimensional set shifting performance following frontal lobe excisions, temporal lobe excisions or amygdalo-hippocampectomy in man
Neuropsychologia
(1991)
S. Monsell
Task switching
Trends Cogn. Sci.
(2003)
M.C. Davidson
Development of cognitive control and executive functions from 4 to 13 years: evidence from manipulations of memory, inhibition, and task switching
Neuropsychologia
(2006)
A.R. Aron
Inhibition and the right inferior frontal cortex
Trends Cogn. Sci.
(2004)
S. Teixeira
Integrative parietal cortex processes: neurological and psychiatric aspects
J. Neurol. Sci.
(2014)
T.D. Wager
Neuroimaging studies of shifting attention: a meta-analysis
Neuroimage
(2004)
N. Schmitz
Neural correlates of executive function in autistic spectrum disorders
Biol. Psychiatry
(2006)
N.U. Dosenbach
A dual-networks architecture of top-down control
Trends Cogn. Sci.
(2008)
L. Pessoa
Understanding brain networks and brain organization
Phys. Life Rev.
(2014)

L.F. Barrett et al.

Large-scale brain networks in affective and social neuroscience: towards an integrative functional architecture of the brain

Curr. Opin. Neurobiol.

(2013)

A.S. Dick

The development of cognitive flexibility beyond the preschool period: an investigation using a modified Flexible Item Selection Task

J. Exp. Child Psychol.

(2014)

N. Chevalier

Qualitative change in executive control during childhood and adulthood

Cognition

(2013)

F. Ezekiel

Dimensional Change Card Sort performance associated with age-related differences in functional connectivity of lateral prefrontal cortex

Dev. Cogn. Neurosci.

(2013)

C. Wendelken

Flexible rule use: common neural substrates in children and adults

Dev. Cogn. Neurosci.

(2012)

M.J. Taylor

fMRI and MEG in the study of typical and atypical cognitive development

Neurophysiol. Clin.

(2012)

E.G. Willcutt

Validity of the executive function theory of attention-deficit/hyperactivity disorder: a meta-analytic review

Biol. Psychiatry

(2005)

J.A. Sergeant

How specific is a deficit of executive functioning for attention-deficit/hyperactivity disorder?

Behav. Brain Res.

(2002)

B.A. Corbett

Examining executive functioning in children with autism spectrum disorder, attention deficit hyperactivity disorder and typical development

Psychiatry Res.

(2009)

K.M. Shafritz

The neural circuitry mediating shifts in behavioral response and cognitive set in autism

Biol. Psychiatry

(2008)

D.D. Garrett

Moment-to-moment brain signal variability: a next frontier in human brain mapping?

Neurosci. Biobehav. Rev.

(2013)

I. Dinstein

Neural variability: friend or foe?

Trends Cogn. Sci.

(2015)

C. Chang et al.

Time–frequency dynamics of resting-state brain connectivity measured with fMRI

Neuroimage

(2010)

R.M. Hutchison

Dynamic functional connectivity: promise, issues, and interpretations

Neuroimage

(2013)

D.J.N. Armbruster

Prefrontal cortical mechanisms underlying individual differences in cognitive flexibility and stability

J. Cogn. Neurosci.

(2012)

W.A. Scott

Cognitive complexity and cognitive flexibility

Sociometry

(1962)

P.M.E. de Abreu

Executive functioning and reading achievement in school: a study of Brazilian children assessed by their teachers as ‘poor readers’

Front. Psychol.

(2014)

J.J. Genet et al.

Flexible control in processing affective and non-affective material predicts individual differences in trait resilience

Cogn. Emot.

(2011)

J.C. Davis

The independent contribution of executive functions to health related quality of life in older women

BMC Geriatr.

(2010)

V. Vilgis

Executive function and attention in children and adolescents with depressive disorders: a systematic review

Eur. Child Adolesc. Psychiatry

(2015)

B. Casey

Early development of subcortical regions involved in non-cued attention switching

Dev. Sci.

(2004)

S. Konishi

Transient activation of inferior prefrontal cortex during cognitive set shifting

Nat. Neurosci.

(1998)

D. Badre et al.

Computational and neurobiological mechanisms underlying cognitive flexibility

Proc. Natl. Acad. Sci. U.S.A.

(2006)

B.E. Yerys

Neural correlates of set-shifting in children with autism

Autism Res.

(2015)

S.A. Bunge et al.

A brain-based account of the development of rule use in childhood

Curr. Direct. Psychol. Sci.

(2006)

L.Q. Uddin

Salience processing and insular cortical function and dysfunction

Nat. Rev. Neurosci.

(2015)

L.Q. Uddin

Dynamic reconfiguration of structural and functional connectivity across core neurocognitive brain networks with development

J. Neurosci.

(2011)

M. Corbetta et al.

Control of goal-directed and stimulus-driven attention in the brain

Nat. Rev. Neurosci.

(2002)

M.E. Thomason

Development of spatial and verbal working memory capacity in the human brain

J. Cogn. Neurosci.

(2009)

B.J. Levy et al.

Cognitive control and right ventrolateral prefrontal cortex: reflexive reorienting, motor inhibition, and action updating

Ann. N. Y. Acad. Sci.

(2011)

A.R. Aron et al.

Cortical and subcortical contributions to stop signal response inhibition: role of the subthalamic nucleus

J. Neurosci.

(2006)

W. Cai

Dissociable roles of right inferior frontal cortex and anterior insula in inhibitory control: evidence from intrinsic and task-related functional parcellation, connectivity, and response profile analyses across multiple datasets

J. Neurosci.

(2014)

W.W. Seeley

Dissociable intrinsic connectivity networks for salience processing and executive control

J. Neurosci.

(2007)

A. Sebastian

Dissociable attentional and inhibitory networks of dorsal and ventral areas of the right inferior frontal cortex: a combined task-specific and coordinate-based meta-analytic fMRI study

Brain Struct. Funct.

(2015)

Cited by (541)

Executive functioning in child victims of sexual abuse: A multi-informant comparative study
2024, Child Abuse and Neglect
Research examining the association between child sexual abuse and executive functions is limited. Yet, exposure to traumatic situations at a young age has been associated with changes in the prefrontal cortex, which hosts executive functions (Wesarg et al., 2020). These functions are crucial for social adaptation, as they make it possible to inhibit maladaptive behavior and respond flexibly to the demands of the environment. As middle childhood is a sensitive period for the development of self-regulatory abilities, exploring executive functioning in school-age children could provide potential intervention targets (Dajani & Uddin, 2015).
Using multiple informants, this study compared executive functioning of sexually abused children to that of non-sexually victimized children and examined whether the differences were moderated by sex.
The sample consisted of 225, 6-to-12 years old children with a history of child sexual abuse (CSA) and 97 children without a history of CSA. Children completed two executive functioning tasks measuring cognitive flexibility and inhibition. Parents and teachers completed questionnaires evaluating children's executive functioning.
In comparison to non-abused children, children with a history of CSA displayed greater executive functioning difficulties as assessed by both informant-reported questionnaires and self-completed tasks. Significant interaction effects were found, such as CSA predicting lower inhibition and executive functions at school in boys but not in girls.
This study is a first step in understanding the association between CSA and executive functioning and offers a clearer picture of the differential impact of sexual trauma according to children's sex.
Neural mechanisms distinguishing two types of cooperative problem-solving approaches: An fNIRS hyperscanning study
2024, NeuroImage
Collaborative cooperation (CC) and division of labor cooperation (DLC) are two prevalent forms of cooperative problem-solving approaches in daily life. Despite extensive research on the neural mechanisms underlying cooperative problem-solving approaches, a notable gap exists between the neural processes that support CC and DLC. The present study utilized a functional near-infrared spectroscopy (fNIRS) hyperscanning technique along with a classic cooperative tangram puzzle task to investigate the neural mechanisms engaged by both friends and stranger dyads during CC versus DLC. The key findings of this study were as follows: (1) Dyads exhibited superior behavioral performance in the DLC task than in the CC task. The CC task bolstered intra-brain functional connectivity and inter-brain synchrony (IBS) in regions linked to the mirror neuron system (MNS), spatial perception (SP) and cognitive control. (2) Friend dyads showed stronger IBS in brain regions associated with the MNS than stranger dyads. (3) Perspective-taking predicted not only dyads’ behavioral performance in the CC task but also their IBS in brain regions associated with SP during the DLC task. Taken together, these findings elucidate the divergent behavioral performance and neural connection patterns between the two cooperative problem-solving approaches. This study provides novel insights into the various neurocognitive processes underlying flexible coordination strategies in real-world cooperative contexts.
Biologically plausible models of cognitive flexibility: merging recurrent neural networks with full-brain dynamics
2024, Current Opinion in Behavioral Sciences
Cognitive flexibility, a cornerstone of human cognition, enables us to adapt to shifting environmental demands. This brain function has been widely explored using computational modeling, although oftentimes these models focus on the operational dimension of cognitive flexibility and do not retain a sufficient level of neurobiological detail to lead to electrophysiological or neuroimaging insights. In this review, we explore recent advances and future directions on neurobiologically plausible computational models of cognitive flexibility. We first cover progress in recurrent neural network models trained to perform flexible cognitive tasks, followed by a discussion on how whole-brain or large-scale brain network models have approached the distributed nature of flexible cognitive functions. Ultimately, we propose here a hybrid framework in which both modeling philosophies converge, advocating for a balanced approach that merges computational power with realistic spatiotemporal dynamics of brain activity, and explore early examples in this direction.
Who are you after psychedelics? A systematic review and a meta-analysis of the magnitude of long-term effects of serotonergic psychedelics on cognition/creativity, emotional processing and personality
2024, Neuroscience and Biobehavioral Reviews
This systematic review and a meta-analysis synthesised the results from contemporary, randomized and non-randomized controlled studies to assess lasting (one week minimum) changes on cognition/creativity, emotional processing and personality from serotonergic psychedelics. PubMed, Embase and PsycInfo were searched in July 2022. Risk of bias was assessed using Rob 2.0 and ROBINS-I. Ten studies met the eligibility criteria which involved 304 participants. No statistically significant effects were found for the majority outcome measures across the three constructs. A meta-analysis of emotional recognition outcomes found an overall significant effect for faster reaction times in the active treatment groups for disgust (SMD=−0.63, 95% CI=[−1.01 to −0.25], I2 = 65%) and sadness (SMD=−0.45, 95% CI=[−0.85 to −0.06], I2 = 60%). Future research should include larger samples, better control conditions, standardized doses and longer follow-up periods to confirm these preliminary findings.
Enhancing cognitive flexibility and working memory in individuals with mild cognitive impairment: Exploring the impact of virtual reality on daily life activities
2024, Geriatric Nursing
Mild Cognitive Impairment (MCI) serving as a transitional stage between normal aging and dementia. This study aimed to explore the impact of virtual reality (VR) on enhancing cognitive flexibility, working memory, and daily life activities. Forty participants diagnosed with MCI were randomly assigned to either an intervention group (N = 20) or a control group (N = 20). Evaluations were at baseline, post-training, and three months post-training using various cognitive assessment tools. Results showed that the VR-based cognitive rehabilitation significantly improved instrumental activities of daily living performance, visual and verbal working memory, and reduced anxiety and depression symptoms. While cognitive flexibility did not exhibit significant improvement, these findings highlight VR interventions as a potential avenue for improving cognitive and functional aspects, and alleviating psychological symptoms in individuals with MCI. Further research with larger sample sizes and extended follow-up periods is recommended to establish the long-term effectiveness of such interventions.
Cognitive flexibility in women who recovered from anorexia nervosa – a model-based approach
2024, Journal of Psychiatric Research
Research findings on cognitive flexibility (CF) functioning in women who recovered from anorexia nervosa (RAN) were found to be inconsistent. This was attributed to the multiple definitions of CF and the diverse measuring tools used to assess it. Applying a deductive approach to explore CF function may address these inconsistencies; thus, we used a model that divides CF into three subtypes, namely, stimulus-response mapping, switching sets and task switching. Additionally, we explored the association between CF subtypes and the disorder’s clinical measures to assess the relation of CF to recovery. Forty-three RAN and 54 healthy controls performed tasks designed to assess CF subtypes based on the model’s division, and the RAN group completed the Eating Disorder Examination Questionnaire. The results showed that the RAN group performed significantly worse than controls only in the stimulus-response mapping subtype. Additionally, there were no correlations between CF subtypes and clinical symptoms or the disorder measures – current and nadir body mass index, age of onset, time since recovery, and disorder duration. In conclusion, the study revealed CF impairment after recovery from AN, specifically in stimulus-response mapping. The variability in performance of the CF subtypes supports the application of a theory-driven perspective viewing CF as a modular ability in RAN. Additionally, CF is unrelated to clinical measures post-recovery and thus may not be used as a criterion for evaluating recovery.

View all citing articles on Scopus

View full text

Trends in Neurosciences

ReviewDemystifying cognitive flexibility: Implications for clinical and developmental neuroscience

Highlights

Section snippets

Significance of cognitive flexibility

Defining and measuring cognitive flexibility

EFs required for cognitive flexibility

Brain networks underlying cognitive flexibility

Delineating a cognitive flexibility network in the context of an ECN

Behavioral trajectories

Executive dysfunction and cognitive inflexibility

Future directions: relating neural flexibility and brain dynamics to cognitive flexibility

Concluding remarks

Acknowledgments

Glossary

Neuroimage

Neuropsychologia

Trends Cogn. Sci.

Neuropsychologia

Trends Cogn. Sci.

J. Neurol. Sci.

Neuroimage

Biol. Psychiatry

Trends Cogn. Sci.

Phys. Life Rev.

Curr. Opin. Neurobiol.

J. Exp. Child Psychol.

Cognition

Dev. Cogn. Neurosci.

Dev. Cogn. Neurosci.

Neurophysiol. Clin.

Biol. Psychiatry

Behav. Brain Res.

Psychiatry Res.

Biol. Psychiatry

Neurosci. Biobehav. Rev.

Trends Cogn. Sci.

Neuroimage

Neuroimage

Prefrontal cortical mechanisms underlying individual differences in cognitive flexibility and stability

J. Cogn. Neurosci.

Cognitive complexity and cognitive flexibility

Sociometry

Executive functioning and reading achievement in school: a study of Brazilian children assessed by their teachers as ‘poor readers’

Front. Psychol.

Flexible control in processing affective and non-affective material predicts individual differences in trait resilience

Cogn. Emot.

The independent contribution of executive functions to health related quality of life in older women

BMC Geriatr.

Executive function and attention in children and adolescents with depressive disorders: a systematic review

Eur. Child Adolesc. Psychiatry

Early development of subcortical regions involved in non-cued attention switching

Dev. Sci.

Transient activation of inferior prefrontal cortex during cognitive set shifting

Nat. Neurosci.

Computational and neurobiological mechanisms underlying cognitive flexibility

Proc. Natl. Acad. Sci. U.S.A.

Neural correlates of set-shifting in children with autism

Autism Res.

A brain-based account of the development of rule use in childhood

Curr. Direct. Psychol. Sci.

Salience processing and insular cortical function and dysfunction

Nat. Rev. Neurosci.

Dynamic reconfiguration of structural and functional connectivity across core neurocognitive brain networks with development

J. Neurosci.

Control of goal-directed and stimulus-driven attention in the brain

Nat. Rev. Neurosci.

Development of spatial and verbal working memory capacity in the human brain

J. Cogn. Neurosci.

Cognitive control and right ventrolateral prefrontal cortex: reflexive reorienting, motor inhibition, and action updating

Ann. N. Y. Acad. Sci.

Cortical and subcortical contributions to stop signal response inhibition: role of the subthalamic nucleus

J. Neurosci.

Dissociable roles of right inferior frontal cortex and anterior insula in inhibitory control: evidence from intrinsic and task-related functional parcellation, connectivity, and response profile analyses across multiple datasets

J. Neurosci.

Dissociable intrinsic connectivity networks for salience processing and executive control

J. Neurosci.

Dissociable attentional and inhibitory networks of dorsal and ventral areas of the right inferior frontal cortex: a combined task-specific and coordinate-based meta-analytic fMRI study

Brain Struct. Funct.

Review
Demystifying cognitive flexibility: Implications for clinical and developmental neuroscience