Elsevier

NeuroImage

Volume 156, 1 August 2017, Pages 199-206
NeuroImage

Taking control! Structural and behavioural plasticity in response to game-based inhibition training in older adults

https://doi.org/10.1016/j.neuroimage.2017.05.026Get rights and content

Highlights

  • We set out to train response inhibition using computer-game elements.

  • We trained older adults for 2 months and had an active and passive control group.

  • The experimental group showed increases in right IFG cortical thickness.

  • The experimental group showed shorter stop signal response times after training.

  • The results may foster treatment research in psychiatric impulse control diseases.

Abstract

While previous attempts to train self-control in humans have frequently failed, we set out to train response inhibition using computer-game elements. We trained older adults with a newly developed game-based inhibition training on a tablet for two months and compared them to an active and passive control group. Behavioural effects reflected in shorter stop signal response times that were observed only in the inhibition-training group. This was accompanied by structural growth in cortical thickness of right inferior frontal gyrus (rIFG) triangularis, a brain region that has been associated with response inhibition. The structural plasticity effect was positively associated with time spent on the training-task and predicted the final percentage of successful inhibition trials in the stop task. The data provide evidence for successful trainability of inhibition when game-based training is employed. The results extend our knowledge on game-based cognitive training effects in older age and may foster treatment research in psychiatric diseases related to impulse control.

Introduction

Self-control is at the heart of human nature and frequently diminished in older age and psychiatric disease. Self-control interrupts the normal flow from intention to action. This ability to prevent and override unwanted thoughts, behaviours or emotions is integral to our functioning in daily life (Muraven et al., 1999), e.g. in traffic when you see that another car swerves into your blind spot just as you are about to switch lanes and you need to hit the brakes, or when trying to be polite during a conversation with a friend and not checking the mobile phone although you hear that a text message has just arrived. In experimental psychology, self-control is usually conceptualized under the construct of inhibition and frequently assessed using behavioural tasks like the stop signal task (Logan and Burkell, 1986). The stop signal task consists of a primary motor task, e.g. responding to a white arrow with a button press. If, however, a stop signal is presented (e.g. colour change to red), the participants are instructed to stop the ongoing motor response. The duration of the inhibition process can be derived from the reaction time data, a measure that has been termed stop signal reaction time (SSRT).

In the literature inhibition has been associated with a consistent network of brain regions comprising most prominently the prefrontal cortex, in particular the right inferior frontal gyrus (rIFG, Aron et al., 2014). The rIFG is reliably activated during inhibition (for a meta-analysis see Swick et al. (2011)), and disruption of its integrity via lesions (Aron et al., 2003) or by means of transcranial magnetic stimulation (Verbruggen et al., 2010) result in substantial increases in SSRT.

Within the scope of the present study, we set out to train externally triggered inhibition. Interestingly, compared to the wealth of knowledge obtained on the training of various executive functions such as working memory (Klingberg, 2010, Kühn et al., 2012a), the literature on training of inhibitory control is relatively sparse. In two early studies, no effect of inhibition training was found (Logan and Burkell, 1986, Cohen and Poldrack, 2008) and several meta-analyses and large scale studies on the training of executive functions show mixed evidence for training effects and little or no evidence for transfer effects (Owen et al., 2010, Melby-Lervåg and Hulme, 2013). The lack of research in this area can most likely be attributed to the fact that inhibition is widely regarded as “untrainable” (Gray et al., 2003). However, recent findings from cognitive neuroscience provide evidence for the existence of training effects. One study used an adaptive stop task design over a training period of three weeks showing decreases in rIFG activation during implementation of control, and increases in lateral prefrontal cortex during the cue phase (Berkman et al., 2014). The authors argue that transfer effects in the domain of inhibition might be difficult to find, because particular contingencies of the cue stimuli are learned, which are highly task specific. Recently, several authors have suggested that training with video games results in surprisingly wide transfer effects (Cardoso-Leite and Bavelier, 2014). In a previous study, we have been able to demonstrate structural changes in a brain network involved in spatial navigation after a two-month training period with a platform game that places high demands on 3D orientation (Super Mario 64), accompanied by changes in an untrained orientation task (Kühn et al., 2013).

Based on this prior evidence, we set out to design a video game-like training task that encompassed elements of response inhibition. Throughout the training intervention, difficulty level was increased by introducing faster switches between the inhibition stimuli and more items that required inhibition. We predicted structural increases in rIFG, based on the abovementioned evidence linking response inhibition to the integrity of rIFG, in particular in rIFG orbitalis and triangularis based on a previous meta-analysis on inhibition tasks (Kühn et al., 2013) and behavioural effects in a classical stop signal task. We selected cortical thickness as the parameter of interest since it has previously been suggested to be a more sensitive parameter with a higher signal-to-noise ratio compared to voxel-based morphometry (Dickerson et al., 2008; Hutton et al., 2009; Salat et al., 2004). Moreover, cortical thickness measures have been considered to be more easily interpretable than the probabilistic grey matter volumes in VBM (Lehmann et al., 2011). Since older age has been associated with a decrease in the capacity to inhibit (Kramer et al., 1994), most likely associated with the widely described age-related decline in the frontal lobe (Fjell et al., 2009), we selected a sample of adults aged 60 and above, where a realistic need to train self-control can be expected.

Section snippets

Participants

Fifty three healthy participants (mean age=69 years, SD=4.2, range 62–78, 27 females) were recruited from the student body of the Senior University, Berlin and by means of flyers and internet advertisements. The advertisement did mention that we were recruiting for a cognitive training study but did not specify which training effects we expected. Moreover participants were randomly assigned to the different groups ruling self-selection effects out. The sample size was based on estimates from a

Results

Participants did not differ between groups in terms of gender (p>0.45), age (p>0.88) or education (p>0.17). On average, participants spent 12.6 h (SD=7.9) ranging from 2.5 to 26.7 hours actively playing the inhibition game and 10.1 h (SD=4.4) ranging from 4 to 16.3 h on the cognitive training platform.

Discussion

Within the scope of the present study we detected structural neural changes as well as behavioural plasticity effects resulting from a tablet-based inhibition-training intervention in older adults. We found structural increase in rIFG triangularis cortical thickness uniquely in the inhibition training group. Moreover, this group showed the strongest behavioural transfer effects to a classical stop signal task as well as a decrease in functional activation of rIFG/anterior insula during stop

Author contribution

S.K., M.W., M.H., J.O'S., A.S., conducted the experiments, S.K., E.S-T., J.G., R.C.L. designed the experiments and wrote the paper, R.C.L. analysed the fMRI data, M.B. analysed the sMRI data, S.B., T.B. programmed the game, all authors read and approved the manuscript.

Conflict of interest

The authors have no conflict of interest.

Acknowledgement

This research has partly been funded by the ERC starting 677804 – Self-Control granted to SK. We are grateful for the assistance of Sonali Beckmann and Nadine Taube operating the scanner as well as the MRI team at the Max Planck Institute for Human Development and the help of our student assistants.

References (43)

  • J.S. Wonderlick et al.

    Reliability of MRI-derived cortical and subcortical morphometric measures: effects of pulse sequence, voxel geometry, and parallel imaging

    NeuroImage

    (2009)
  • A.R. Aron et al.

    Stop-signal inhibition disrupted by damage to right inferior frontal gyrus in humans

    Nat. Neurosci.

    (2003)
  • E.T. Berkman et al.

    Training-induced changes in inhibitory control network activity

    J. Neurosci.

    (2014)
  • A.T. Biggs et al.

    Cognitive training can reduce civilian casualties in a simulated shooting environment

    Psychol. Sci.

    (2015)
  • P. Cardoso-Leite et al.

    Video game play, attention, and learning

    Curr. Opin. Neurol.

    (2014)
  • C.F. Chavan et al.

    Differential patterns of functional and structural plasticity within and between inferior frontal gyri support training-induced improvements in inhibitory control proficiency

    Hum. Brain Mapp.

    (2015)
  • J.R. Cohen et al.

    Automaticity in motor sequence learning does not impair response inhibition

    Psychon. Bull. Rev.

    (2008)
  • J.P. Coxon et al.

    Functional brain activation associated with inhibitory control deficits in older adults

    Cereb. Cortex

    (2016)
  • Dickerson, B.C., Fenstermacher, E., Salat, D.H., Wolk, D.A., Maguire, R.P., Desikan, R., Pacheco, J., Quinn, B.T., Van...
  • Ditye, T., Jacobson, L., Walsh, V., Lavidor, M., 2012. Modulating behavioral inhibition bytDCS combined with cognitive...
  • R. Drobetz et al.

    Structural brain correlates of delay of gratification in the elderly

    Behav. Neurosci.

    (2014)
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