The neurophysiological basis of reward effects on backward inhibition processes
Introduction
In many daily situations we are required to switch between different tasks. Yet, this switching goes along with performance costs, i.e. slower responses and higher error rates. For successful task switching, both an efficient activation of a new task and an inhibition of the no longer relevant previous task are important (Allport et al., 1994, Jamadar et al., 2010, Mayr and Keele, 2000). The process that inhibits the most recently performed task upon switching to a new one is referred to as backward inhibition (BI), and serves the suppression of interferences arising from previous tasks (Allport et al., 1994, Allport and Wylie, 1999, Costa and Friedrich, 2012, Mayr and Keele, 2000). A stronger BI is thought to be related to a better task-switching performance, as it facilitates the activation of a new task set (Mayr and Keele, 2000). However, a strong BI can also be disadvantageous, since the inhibition of a currently irrelevant task can persist over time making it difficult to perform a previously inhibited task when it becomes relevant again (Allport et al., 1994, Allport and Wylie, 1999). To examine these processes, experimental paradigms assessing the time costs of overcoming the inhibition of a recently abandoned task set which becomes relevant again have been developed to measure task set inhibition (Mayr and Keele, 2000). Performance costs related to BI are observed in task sequences in which a task A is repeated from n-2 trials (e.g. ABA task triplet/BI condition), compared to when that task A has no n-2 trial sequence history (e.g. CBA task triplet/non-BI condition).
Executive control functions are generally known to be modulated by reward manipulations and it has been shown that rewards improve performance in many kinds of cognitive control tasks (Braem et al., 2012, Libera and Chelazzi, 2006, Veling and Aarts, 2010). In this context, Notebaert and Braem (2015) proposed that different reward components are associated with different kinds of cognitive control behavior: While the hedonic aspect of reward promotes explorative behavior and flexibility, the learning component of reward induces exploitative behavior increasing stability, and the motivational component of reward promotes anticipatory behavior (Notebaert and Braem, 2015). With regard to task switching, some studies showed that reward can reduce the switch costs (Kleinsorge and Rinkenauer, 2012, Savine et al., 2010, Shen and Chun, 2010). As BI is central to the “magnitude” of emerging switch costs, it seems that BI effects should be modulated by rewards as well. Yet, evidence for this assumption is sparse: Jiang and Xu (2014) reported that reward modulates inhibitory processes underlying task switching but they do not provide insights into the underlying neurophysiological mechanisms and functional neuroanatomical structures. In the current study, we combine EEG (event-related potentials, ERPs) with source localization techniques (i.e., sLORETA) to answer the question which neurophysiological processes within the processing cascade from early attentional processes to response selection mechanisms are changed in timing or intensity by reward modulation of the BI effect and what functional neuroanatomical networks are involved. In this context, it needs however to be mentioned that we used a between-subject manipulation with two different group conditions (i.e. performance-based reward for every trial vs. no reward for any trial) whereas the reward schedule of Jiang and Xu, randomly rewarded one third of their trials indicating reward trials with an additional monetary symbol (Jiang and Xu, 2014), With respect to the theory by Notebaert and Braem (2015), we investigated the effects of motivation/reward anticipation while Jiang and Xu investigated the effects of reinforcement history. It is known that reward modulates conflict monitoring and response selection processes (Braem et al., 2012, Krebs et al., 2013). Compared to the non-BI condition (CBA), the reactivation of the recently abandoned task intensifies response selection and conflict monitoring processes and causes a conflict indicating the need for additional allocation of control in the BI condition (ABA). However, the exertion of this control is assumed to carry an inherent subjective cost. As a consequence, the exertion of cognitive control depends on the expected value of control. In other words, the allocation of control is driven by a cost-benefit analysis which is likely to be modulated by rewards (Shenhav et al., 2013). Based thereon, we expect that rewards affect the BI and non-BI condition differently. Inasmuch as the N2 component has been demonstrated to reflect cognitive control and conflict monitoring processes (Botvinick et al., 2004, Deng et al., 2015, Donkers and van Boxtel, 2004, Folstein and Van Petten, 2008, Huster et al., 2013, Larson et al., 2014), we expect that the N2 component shows relevant differences related to the reward modulation of the BI effect. The anterior cingulate cortex (ACC) is highly associated with conflict-related N2 (Folstein and Van Petten, 2008, Yeung and Cohen, 2006). It plays an important role in conflict monitoring and in assessing the need for cognitive control (Botvinick et al., 2004, Cavanagh and Frank, 2014, Folstein and Van Petten, 2008, Holroyd and McClure, 2015, Kerns et al., 2004, Shenhav et al., 2013). Hence, reward-related modulations of the BI effect should be associated with the ACC. Yet, reward is supposed to have effects on attentional processes as well: It has been shown that the N1 and P2 components are modulated by reward, suggesting changes in attentional processes and the distinctive allocation of attentional resources (Chmielewski et al., 2015, Doñamayor et al., 2012, Flores et al., 2015, Stock et al., 2015, Sugimoto and Katayama, 2013, Yu and Zhou, 2006). Based thereon, it is possible that attentional selection processes during backward inhibition are also modulated by rewards. Matching this, the N1, which is known to reflect attentional selection processes (Beste et al., 2010, Gajewski et al., 2013, Herrmann and Knight, 2001, Luck et al., 1990, Wascher and Beste, 2010), has been demonstrated to be larger in the BI condition than in the control condition (Sinai et al., 2007). This suggests that attentional selection processes in the BI condition are intensified to re-activate the recently abandoned task, which makes it possible that these mechanisms are also modulated by rewards. Given that dopaminergic innervation, which also carries reward signals (e.g. Schultz, 1998), is less strong in occipital and parietal areas than in medial frontal (ACC) regions (Nieoullon, 2002), it is however possible that attentional processes show less reward modulation effects than response selection and conflict monitoring processes.
Another process which could be involved in backward inhibition is reflected by the P3 ERP. During task switching, the P3 has been linked to processes of context-updating and stimulus-response re-mapping (e.g. Finke et al., 2012, Gajewski and Falkenstein, 2011, Polich, 2007). Given that the BI effect arises in the situation, where a recently abandoned task becomes relevant again, it is possible that the BI effect relates to difficulties in context-updating and the decision of stimulus-response mapping, which can be reflected in the P3. Some studies found that the P3 components are also modulated by the reward, which has been ascribed to the increased attention to reward predictive cues (Krebs et al., 2013) and the updating of the internal environment (Broyd et al., 2012, Flores et al., 2015, Gruber and Otten, 2010). On these grounds, we expected that reward modulation might be shown in the P3 components.
Section snippets
Participants
N = 56 healthy subjects between 18 and 30 years of age took part in the experiment. Participants were allocated to a control group (mean age of 23.7 ± 3.3; 18 females, 10 males) and a reward group (mean age of 23.6 ± 3.2; 18 females, 10 males) which were matched for sex and age. All participants were right-handed, had normal or corrected-to-normal vision and no history of neurological or psychiatric disorders. Written informed consent was obtained from all participants at the beginning of the
Reward
Participants in the reward group gained a reward varying from 10.74€ to 14.70€ (mean reward: 12.60€ ± 0.22), while participants in the control group got a fixed payment of 7.50€.
Backward inhibition effect
To examine the BI effect, we paired each back-switching triplet with its respective baseline triplet (which only differed in the n-2 trial cue). According to the study of Koch et al. (Koch et al., 2004), BI effects only emerge when previous (n-1) trials require choice Go responses. Moreover, the BI effect interacts with
Discussion
In the current study, we investigated whether the backward inhibition (BI) effect, a mechanism assumed to central for task switching processes, is modulated by performance-related rewards. A modulation of the BI effect by reward can be observed in the RT data: Participants in the reward group exhibited a smaller BI effect than those in the control group. Notably, the neurophysiological data parallels this behavioral interaction showing that reward modulates the BI effect as reflected by
Conclusions
In summary, our study examines the neurophysiological mechanisms underlying reward-related changes in backward inhibition during task switching. The results show that rewards reduce the magnitude of backward inhibition, probably by increasing the invested cognitive effort and/or reducing switch costs associated with BI. The neurophysiological data shows that these reward-related effects emerge from a specific modulation of response and/or conflict monitoring processes in medial frontal cortical
Acknowledgements
This work was supported by a grant from the German Research Foundation (DFG) awarded to C.B. (BE4045/10-2).
References (82)
- et al.
What is the role of dopamine in reward: hedonic impact, reward learning, or incentive salience?
Brain Res. Brain Res. Rev.
(1998) - et al.
Conflict monitoring and anterior cingulate cortex: an update
Trends Cogn. Sci.
(2004) - et al.
Reward modulates adaptations to conflict
Cognition
(2012) - et al.
An electrophysiological monetary incentive delay (e-MID) task: a way to decompose the different components of neural response to positive and negative monetary reinforcement
J. Neurosci. Methods
(2012) - et al.
Long-lasting effects of performance-contingent unconscious and conscious reward incentives during cued task-switching
Cortex J. Devoted Study Nerv. Syst. Behav.
(2013) - et al.
Frontal theta as a mechanism for cognitive control
Trends Cogn. Sci.
(2014) - et al.
A review of the evidence for P2 being an independent component process: age, sleep and modality
Clin. Neurophysiol.
(2004) - et al.
Magneto- and electroencephalographic manifestations of reward anticipation and delivery
NeuroImage
(2012) - et al.
The N2 in go/no-go tasks reflects conflict monitoring not response inhibition
Brain Cogn.
(2004) - et al.
Event-related EEG responses to anticipation and delivery of monetary and social reward
Biol. Psychol.
(2015)
A standardized boundary element method volume conductor model
Clin. Neurophysiol. Off. J. Int. Fed. Clin. Neurophysiol.
Diversity of the P3 in the task-switching paradigm
Brain Res.
The functional tumor necrosis factor-α (308A/G) polymorphism modulates attentional selection in elderly individuals
Neurobiol. Aging
Revisiting the oddball paradigm. Non-target vs neutral stimuli and the evaluation of ERP attentional effects
Neuropsychologia
Mechanisms of human attention: event-related potentials and oscillations
Neurosci. Biobehav. Rev.
Electroencephalography of response inhibition tasks: functional networks and cognitive contributions
Int. J. Psychophysiol.
The spatial and temporal dynamics of anticipatory preparation and response inhibition in task-switching
NeuroImage
Making sense of all the conflict: a theoretical review and critique of conflict-related ERPs
Int. J. Psychophysiol. Off. J. Int. Organ. Psychophysiol.
Visual event-related potentials index focused attention within bilateral stimulus arrays. II. Functional dissociation of P1 and N1 components
Electroencephalogr. Clin. Neurophysiol.
Dopamine and the regulation of cognition and attention
Prog. Neurobiol.
Temporal difference models and reward-related learning in the human brain
Neuron
Updating P300: an integrative theory of P3a and P3b
Clin. Neurophysiol. Off. J. Int. Fed. Clin. Neurophysiol.
More attention must be paid: the neurobiology of attentional effort
Brain Res. Rev.
Reward prediction in primate basal ganglia and frontal cortex
Neuropharmacology
Localization bias and spatial resolution of adaptive and non-adaptive spatial filters for MEG source reconstruction
NeuroImage
The expected value of control: an integrative theory of anterior cingulate cortex function
Neuron
Somatosensory P2 reflects resource allocation in a game task: assessment with an irrelevant probe technique using electrical probe stimuli to shoulders
Int. J. Psychophysiol. Off. J. Int. Organ. Psychophysiol.
Task-switching: positive and negative priming of task-set
Shifting intentional set: exploring the dynamic control of task
Variations in the TNF-α gene (TNF-α-308G → A) affect attention and action selection mechanisms in a dissociated fashion
J. Neurophysiol.
Motivation and cognitive control: from behavior to neural mechanism
Annu. Rev. Psychol.
Concurrent information affects response inhibition processes via the modulation of theta oscillations in cognitive control networks
Brain Struct. Funct.
Analyzing Neural Time Series Data: Theory and Practice
Inhibition, interference, and conflict in task switching
Psychon. Bull. Rev.
Conflict monitoring and adjustment in the task-switching paradigm under different memory load conditions: an ERP/sLORETA analysis
Neuroreport
A causal role of the right inferior frontal cortex in implementing strategies for multi-component behaviour
Nat. Commun.
The effects of foreknowledge and task-set shifting as mirrored in cue- and target-locked event-related potentials
PLoS One
Influence of cognitive control and mismatch on the N2 component of the ERP: a review
Psychophysiology
Prefrontal and striatal dopaminergic genes predict individual differences in exploration and exploitation
Nat. Neurosci.
The importance of sensory integration processes for action cascading
Sci. Rep.
Temporal cue-target overlap is not essential for backward inhibition in task switching
Q. J. Exp. Psychol.
Cited by (31)
Distinct Brain-Oscillatory Neuroanatomical Architecture of Perception-Action Integration in Adolescents With Tourette Syndrome
2021, Biological Psychiatry Global Open ScienceEffects of food stimuli on event-related potentials of restrained eating subgroups during task switching
2021, Neuroscience LettersCitation Excerpt :In the present study, the N2 amplitude of UREs was larger than SREs, it converges with the results of research on ex-obese adults, wherein participants are required to monitor and solve a conflict generated by the habitual and the required response [25]. In previous studies, N2 and target-P3 amplitudes have been demonstrated to be highly correlated during task switching [28]. The positive ERP component at parietal electrode sites evoked approximately 400 ms after the presentation of the cue to switch showed significantly pronounced amplitude among UREs compared to SREs, also in food or switch trials.
A possible role of the norepinephrine system during sequential cognitive flexibility – Evidence from EEG and pupil diameter data
2020, CortexCitation Excerpt :Within these segments, an automated artifact rejection procedure was conducted (criteria: amplitude differences above 200 μV in a 200 ms time interval, activity below .5 μV in a 100 ms time period). For a reference-free evaluation of the data, a current source density (CSD) transformation was run (Kayser & Tenke, 2015), as done in previous studies using the backward inhibition task (Wolff et al., 2018; Zhang, Stock, & Beste, 2016; Zhang, Stock, Fischer, et al., 2016). Following that, a baseline correction was performed in the interval of −200 to 0 ms before cue onset.
- 1
These authors contributed equally.