Lower theta inter-trial phase coherence during performance monitoring is related to higher reaction time variability: A lifespan study
Introduction
Cross-sectional studies have repeatedly reported that within-person trial-to-trial reaction time (RT) variability decreases from childhood to adolescence and increases again from young adulthood to old age (e.g., Dykiert et al., 2012, Li et al., 2004, Li et al., 2009, Williams et al., 2005, Williams et al., 2007). Intra-individual variability in reaction times is generally considered to be an index of central nervous system functioning (for a recent review, see Dykiert et al., 2012). Previous research has shown that elevated RT variability reflects the efficacy of higher level cognitive functioning above and beyond motor executive processes. For instance, RT variability in older adults has been attributed to the decision rather than the motor component of a task (e.g., Bunce et al., 2004). Moreover, higher trial-to-trial RT variability is associated with lower behavioral performance in a variety of complex cognitive tasks (e.g., Hultsch et al., 2002) and has been shown to predict longitudinal cognitive decline in late adulthood, such as in executive functioning (Lövdén et al., 2007) and episodic memory (MacDonald et al., 2003).
In clinical research, deficiency in frontal lobe functioning has been related to higher processing fluctuations. Adult patients with lesions in the frontal lobes usually show more variable RTs in comparison to healthy controls (Murtha et al., 2002, Picton et al., 2007, Stuss et al., 2003, Walker et al., 2000). In healthy adult samples, age differences are particularly pronounced on tasks assessing frontal lobe functioning, such as inhibition (Strauss et al., 2007) and working memory (West et al., 2002; Dixon et al., 2007). Similarly, children with frontal-lobe mediated executive control deficits, such as patients with attention deficit hyperactivity disorder, show higher RT variability than healthy controls (for review, see Kuntsi and Klein, 2012). Indeed, structural, functional and neurochemical declines in the frontal lobes in old age (for reviews, see MacDonald et al., 2006, MacDonald et al., 2009) have been associated with higher within-person variability. However, the functional processes underlying the contribution of the frontal lobe to higher RT fluctuations remain poorly understood.
Three decades of cognitive neuroscience research have established the role of the medial frontal cortex (MFC) in performance monitoring and cognitive control (for review, see Ridderinkhof et al., 2004). More recent investigations on cognitive control suggest that the MFC exerts control by interacting with other task relevant brain regions through neural oscillations in the theta (4–7 Hz) band (e.g., Cavanagh et al., 2009, Cohen et al., 2011, Hanslmayr et al., 2008, Nigbur et al., 2012). Direct intracranial recordings confirm the MFC as a generator of theta band oscillations in humans (Cohen et al., 2008, Wang et al., 2005). Specifically, Cohen and colleagues found that performance during a modified Flanker task was associated with an enhancement of theta power following the response suggesting post-response performance monitoring. In addition, theta oscillations in the MFC and fronto-central scalp electrodes were coupled, indicating that scalp electrodes indeed reflect activity from intracranial sources. In line with the suggested role in cognitive control and monitoring, increases in medial frontal theta band power have been observed in more demanding performance monitoring conditions, such as during Go/NoGo tasks (e.g., Nigbur et al., 2011, Schmiedt-Fehr and Basar-Eroglu, 2011). Furthermore, medial frontal theta activity has been consistently observed to be higher during situations requiring more cognitive control, such as during errors or prior to performance adaptations (e.g., Cavanagh et al., 2012, Cohen et al., 2008, Cohen et al., 2009, Luu and Tucker, 2002, Mazaheri et al., 2009).
Other than amplitude-related measures, the temporal synchronicity of theta oscillations has recently gained more attention in the research on cognitive control. It has been suggested that variability in the stimulus-locked theta phase across trials at single electrodes or between electrodes presumably reflects the temporal coordination of cortical processes (Klimesch et al., 2007, Sauseng and Klimesch, 2008). Given that the theta oscillation is a promising neural correlate for frontally coordinated cognitive control processes, the phase of the oscillation might provide a means for coordinating interactions between distant brain areas (e.g., Cavanagh et al., 2009, Cohen et al., 2011). Of specific relevance for the current study, increasing evidence shows that lower theta inter-trial phase locking at single electrodes is related to behavioral performance (e.g., Klimesch et al., 2004, Groom et al., 2010; Müller et al., 2009, Rutishauser et al., 2010). Specifically, higher RT variability in a Go/NoGo task has been found to be associated with lower inter-trial phase coherence in the theta band in adolescents (Groom et al., 2010), indicating that increased intraindividual variability may be related to more variable electroencephalographic signals in the theta range. However, participants in the Groom et al. (2010) study motorically responded during the condition of interest; therefore, lower coherence in this case may not necessarily reflect variability in higher-level control processes, as lower theta coherence could also have reflected neural variability associated with motor execution processes. To summarize, interindividual differences in RT variability may be due to deficient frontal cognitive control processing. Initial evidence suggests that temporal variability in performance monitoring in the MFC might be a suitable candidate process for studying lifespan developmental and individual differences in behavioral RT variability.
Given the involvement of the MFC in performance monitoring and motor control that is well-established in functional brain imaging studies (for review, see Ridderinkhof et al., 2004), we aimed at investigating whether more variable performance monitoring signals, which are not confounded with motor responses, would be associated with greater variability in response latencies of behavior and brain electrophysiological responses. In addition, we aimed at investigating whether lifespan age differences in RT variability are also reflected in lifespan age differences in the temporal variability of performance monitoring processes.
We analyzed event-related theta oscillations assessed during a cued Go/NoGo task in a lifespan sample (children, adolescents, younger adults, older adults) with a specific focus on inter-trial phase coherence (ITPC). Based on initial evidence relating lower theta ITPC to higher RT variability (Groom et al., 2010) and the well-established lifespan patterns of RT variability (e.g., Li et al., 2004, Williams et al., 2005), we expected an increase in theta NoGo ITPC with maturation and a decrease in old age. Here, we focus particularly on the NoGo condition, as performance monitoring demands are highest in this condition and Go trials may be confounded with response-related activity. Further, we expected that within age groups variability of performance monitoring signals would predict individual differences in behavioral variability. Specifically, we expected that individuals with higher theta inter-trial phase synchrony during the NoGo condition show higher behavioral RT variability. In addition, it remains an open question whether theta power would also predict RT variability. Thus, we further tested whether the magnitude of the theta response would also be predictive of interindividual differences in RT variability or whether the link to behavioral variability is specific to the coherence measure.
Section snippets
Participants
The sample included 182 participants, with 35 children (aged 9 to 11 years; 21 girls), 43 adolescents (aged 12 to 16 years; 22 girls), 46 younger (aged 20 to 28 years; 22 women), and 47 older adults (aged 65 to 75 years; 24 women). Data from 10 children and 1 adolescent were excluded due to an insufficient number of available trials after artifact rejections for time–frequency analyses (i.e., fewer than 25 trials per condition). All participants were right-handed, as indexed by the Edinburgh
Lifespan differences in trial-to-trial RT variability
RT variability during the Go condition is presented in Fig. 1 for the four age groups. The omnibus test yielded a main effect of age group, F(3,76.2) = 35.2, p < .05, ICC = 0.76 (explaining 58% of the total variance in the data). Planned contrasts confirmed a linear, t = 8.84, p < .05, d = 1.76, and curvilinear pattern, t = 8.31, p < .05, d = 1.35, across the lifespan. In line with the curvilinear pattern, pairwise comparisons indicated that adolescents were less variable in their RTs than children, t = 2.43, p <
Discussion
Here, we investigated whether EEG correlates of more variable performance monitoring signals in the MFC may be related to higher RT variability in a lifespan sample. We found that variability in stimulus-locked EEG signals during performance monitoring is higher at both ends of the lifespan, as indicated by theta ITPC during NoGo trials. This pattern was paralleled by lifespan differences in behavioral variability, with decreasing RT variability from childhood to young adulthood and increasing
Acknowledgments
This research was supported by the German Research Foundation's (DFG) grant for a subproject (Li 515/8-1 to S.-C. L., V. M. and U. L.) in the research group on Conflicts As Signals (DFG FOR778). D. H. was a Ph.D. and postdoctoral fellow supported by this grant. G. P. is a fellow of the International Max Planck Research School, The Life Course: Evolutionary and Ontogenetic Dynamics (LIFE). The manuscript was completed while D. H. was a visiting postdoctoral fellow at the University College
References (62)
- et al.
Inconsistency in serial choice decision and motor reaction times dissociate in younger and older adults
Brain Cogn.
(2004) - et al.
Medial frontal cortex and response conflict: evidence from human intracranial EEG and medial frontal cortex lesion
Brain Res.
(2008) - et al.
Cortical electrophysiological network dynamics of feedback learning
Trends Cogn. Sci.
(2011) - et al.
EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis
J. Neurosci. Meth.
(2004) - et al.
The effect of the skull on event-related P300
Clin. Neurophysiol.
(2001) - et al.
An electrophysiological study of response conflict processing across the lifespan: assessing the roles of conflict monitoring, cue utilization, response anticipation, and response suppression
Neuropsychologia
(2010) - et al.
Phase-locked alpha and theta oscillations generate the P1–N1 complex and are related to memory performance
Cogn. Brain Res.
(2004) - et al.
EEG alpha oscillations: the inhibition-timing hypothesis
Brain Res. Rev.
(2007) - et al.
Within-person trial-to-trial variability precedes and predicts cognitive decline in old and very old age: longitudinal data from the Berlin Aging Study
Neuropsychologia
(2007) - et al.
Intra-individual variability in behavior: links to brain structure, neurotransmission and neuronal activity
Trends Neurosci.
(2006)
Theta power as a marker for cognitive interference
Clin. Neurophysiol.
The assessment and analysis of handedness: the Edinburgh inventory
Neuropsychologia
Frontal midline EEG dynamics during working memory
Neuroimage
What does phase information of oscillatory brain activity tell us about cognitive processes?
Neurosci. Biobehav. Rev.
Control mechanisms in working memory: a possible function of EEG theta oscillations
Neurosci. Biobehav. Rev.
Event-related delta and theta brain oscillations reflect age-related changes in both a general and a specific neuronal inhibitory mechanism
Clin. Neurophysiol.
Rhythmic TMS causes local entrainment of natural oscillatory signatures
Curr. Biol.
Lapses of intention and performance variability reveal age-related increases in fluctuations of executive control
Brain Cogn.
Inconsistency in reaction time across the life span
Neuropsychology
A continuous performance test of brain damage
J. Consult. Clin. Psychol.
Anterior cingulate cortex and response conflict: effects of frequency, inhibition and errors
Cereb. Cortex
Prelude to and resolution of an error: EEG phase synchrony reveals cognitive control dynamics during action monitoring
J. Neurosci.
Theta lingua franca: a common mid-frontal substrate for action monitoring processes
Psychophysiology
Single-trial regression elucidates the role of prefrontal theta oscillations in response conflict
Front. Psychol.
Unconscious errors enhance prefrontal–occipital oscillatory synchrony
Front. Hum. Neurosci.
Neurocognitive resources in cognitive impairment: exploring markers of speed and inconsistency
Neuropsychology
Sex differences in reaction time mean and intraindividual variability across the life span
Dev. Psychol.
Effect-size estimates: issues and problems in interpretation
J. Consum. Res.
Electrophysiological indices of abnormal error-processing in adolescents with attention deficit hyperactivity disorder (ADHD)
J. Child Psychol. Psychiatry
The electrophysiological dynamics of interference during the Stroop task
J. Cogn. Neurosci.
Variability in reaction time performance of younger and older adults
J. Gerontol. B Psychol. Sci. Soc. Sci.
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- 1
Present address: Aging Research Center, Karolinska Institute, S-11330 Stockholm, Sweden.
- 2
Shared first authorship.