B8
Functional neuroanatomical and neurobiological modulators of the interaction of volitionally controlled and automatic behavior
PROJECT AIMS
Volitional control and automaticity have long been considered as opposing processes. In this context, volitional control has long often been described as a superior faculty mainly used to modify automatic behavior. Yet, there is mounting evidence that volitional control and automaticity seem to interact in both directions. While there has been much research on this interaction at the behavioral level, the underlying neural mechanisms have remained rather elusive. Against this background, project B8 investigates key functional neuroanatomical and neurobiological mechanisms associated with the interaction of volitional control and automatic processes. On the neuroanatomical level, we mainly focus on the functional role of fronto-striatal loops. Concerning neurobiological mechanisms, we take a special interest in the functional relevance of catecholaminergic transmitter systems, GABA, and glutamate. To examine the effects of potential modulators on the interaction between automaticity and control, we use EEG techniques, which are combined with complementary methodological approaches.
RECENT FINDINGS
We were able to demonstrate that automatic response tendencies functionally interact with top-down control processes and further modulate attentional processes (Stock et al. 2016) and that this may be different in neuropsychiatric disorders characterized by cognitive control deficits (Gohil et al. 2017). On the neurophysiological level, we found that theta-mediated cognitive control reflects both consciously and automatically processed response conflicts, but only automatic response tendencies reduce the efficiency of the connectivity of theta-controlled networks (Bensmann et al. 2019). Negative effects of cognitive control on automatic/implicit learning are associated with a greater efficiency of theta-based networks, which probably hinders the exploration of implicit information (Zink et al. 2018). Using a newly developed paradigm (Chmielewski & Beste 2017), we demonstrated that the interaction of automatic and controlled processes occurs primarily at the level of response selection (Chmielewski et al. 2018), which is reflected by mid-frontal theta oscillations (Mückschel et al. 2017).
We could demonstrate that control-relevant stimulus and response codes found in theta oscillations are both processed in the SMA, while the inferior frontal cortex seems to selectively process only the response selection codes (Mückschel et al. 2017). This is in line with control-related, IFG-induced reductions in automaticity and exploration (Stock et al. 2016). Also, we found ACC activation to reflect the interaction of automaticity and control as well as metacontrol/demand-dependent allocation of control (Chmielewski & Beste 2017; Zink et al. 2018). In addition to these cortical areas, we found microstructural properties of the striatum to modulate the interplay of controlled and automatic information conflict processing (Beste et al. 2017).
With respect to the functional role of GABA, we found that experimentally induced changes in its release affect different behavioral measures of controlled behavior to various extents, depending on the task (Beste et al. 2016). Aside from GABA, we examined the role of dopamine/catecholamines using various approaches: We found that latent toxoplasmosis, which is thought to permanently increase dopamine synthesis, may improve cognitive control, but also seems to reduce reward sensitivity (Stock et al. 2017). Furthermore, individuals with a genetic disposition for lower striatal dopamine levels showed larger beneficial effects of experimentally induced increases in dopamine synthesis onto controlled behavior (Colzato et al. 2016). Lastly, we found that experimentally induced increases in catecholaminergic signaling modulate controlled processes more strongly than automatic ones (Bensmann et al. 2018). Yet, the size and direction of catecholamine effects on cognitive control seems to depend on both, control demands and the degree of response automatization / prior task experience (Bensmann et al. 2019). We also observed that alcohol, which shifts the balance of control and automatic processes towards the latter via alterations of GABAergic and dopaminergic neurotransmission (Stock 2017), seems to do so mainly by impairing control, but not as much by altering or improving automatic processes (Wolff et al. 2016; Chmielewski et al. 2018; Zink et al. 2019). We also examined the functional role of norepinephrine and showed that the effects of norepinephrine during cognitive control tasks depend on the saliency and frequency of control-relevant stimulus events (Dippel et al. 2017; Colzato et al. 2017). Norepinephrine further modulates the effects of cognitive load on control processes (Chmielewski et al. 2017) and improves the preparation of cognitive control processes, especially with respect to response preparation (Mückschel et al. 2017; Mückschel et al. 2017; Wolff et al. 2017). Importantly, we recently also found that anodal tDCS of prefrontal structures may eliminate neuromodulatory effects of norepinephrine on control-associated theta band activity, as both the norepinephrinergic system and tDCS seem to modulate neuronal gain control mechanisms (Adelhöfer et al. 2019).
Project Members
Principal Investigators
Prof. Dr. rer. nat. Christian Beste
Professor (W2)
Phone: +49 (0)351 458-7072
E-Mail:
Prof. Dr. med. Veit Roessner
Professor
Phone: +49 (0)351 458-2244
E-Mail:
Dr. rer. nat. Ann-Kathrin Stock
Phone: +49 (0)351 458-4259
E-Mail:
Staff
Anna Helin Koyun Predoc Tel.: +49 (0)351 458-2303
PUBLICATIONS
- Jamous, R., Takacs, A., Frings, C., Mückschel M., Beste C. (2023). Unsigned surprise but not reward magnitude modulates the integration of motor elements during actions. Sci Rep 13, 5379. https://doi.org/10.1038/s41598-023-32508-5
- Wendiggensen P., Beste C. (2023). How Intermittent Brain States Modulate Neurophysiological Processes in Cognitive Flexibility. J Cogn Neurosci. 1;35(4):749-764.https://doi.org/10.1162/jocn_a_01970
- Zhang C., Stock A.K. , Mückschel M., Hommel B., Beste C. (2023). Aperiodic neural activity reflects metacontrol. Cereb Cortex; bhad089. https://doi.org/10.1093/cercor/bhad089
- Eggert, E., Prochnow, A., Roessner, V. et al. (2022). Cognitive science theory-driven pharmacology elucidates the neurobiological basis of perception-motor integration. Commun Biol 5, 919. https://doi.org/10.1038/s42003-022-03864-1
-
Pscherer, C., Mückschel, M., Bluschke, A. et al. (2022). Resting-state theta activity is linked to information content-specific coding levels during response inhibition. Sci Rep 12, 4530. https://doi.org/10.1038/s41598-022-08510-8
- Colzato, L.S., Beste, C. & Hommel, B. (2022). Focusing on cognitive potential as the bright side of mental atypicality. Commun Biol 5, 188. https://doi.org/10.1038/s42003-022-03126-0
- Vahid, A., Mückschel, M., Stober, S. et al. (2022). Conditional generative adversarial networks applied to EEG data can inform about the inter-relation of antagonistic behaviors on a neural level. Commun Biol 5, 148. https://doi.org/10.1038/s42003-022-03091-8
- Colzato LS., Hommel B., Beste C. (2021). The Downsides of Cognitive Enhancement. Neuroscientist. 2021 Aug;27(4):322-330. https://doi.org/10.1177/1073858420945971
- Beste, C. (2021). Disconnected psychology and neuroscience—implications for scientific progress, replicability and the role of publishing. Commun Biol 4, 1099. https://doi.org/10.1038/s42003-021-02634-9
- Adelhöfer, Nico, et al. (2021). "The dynamics of theta-related pro-active control and response inhibition processes in AD (H) D." NeuroImage: Clinical 30 (2021): 102609. https://doi.org/10.1016/j.nicl.2021.102609
- Pscherer, Charlotte, et al. (2021). "The interplay of resting and inhibitory control‐related theta‐band activity depends on age." Human Brain Mapping (2021). https://doi.org/10.1002/hbm.25469
- Prochnow, Astrid, Moritz Mückschel, and Christian Beste. (2021). "Pushing to the Limits: What Processes during Cognitive Control are Enhanced by Reaction–Time Feedback?." Cerebral Cortex Communications 2.2 (2021): tgab027. https://doi.org/10.1093/texcom/tgab027
- Mückschel, Moritz, et al. (2020). "Learning experience reverses catecholaminergic effects on adaptive behavior." International Journal of Neuropsychopharmacology 23.1 (2020): 12-19. https://doi.org/10.1093/ijnp/pyz058
- Adelhöfer, Nico, and Christian Beste. (2020). "Pre-trial theta band activity in the ventromedial prefrontal cortex correlates with inhibition-related theta band activity in the right inferior frontal cortex." Neuroimage 219 (2020): 117052. https://doi.org/10.1016/j.neuroimage.2020.117052
- Colzato, Lorenza S., Bernhard Hommel, and Christian Beste. (2020). "The downsides of cognitive enhancement." The Neuroscientist 27.4 (2021): 322-330. https://doi.org/10.1177/1073858420945971
- Pscherer, Charlotte, et al. (2020). "Resting theta activity is associated with specific coding levels in event‐related theta activity during conflict monitoring." Human brain mapping 41.18 (2020): 5114-5127. https://doi.org/10.1002/hbm.25178
- Adelhöfer, Nico, Marie Luise Schreiter, and Christian Beste. (2020). "Cardiac cycle gated cognitive-emotional control in superior frontal cortices." NeuroImage 222 (2020): 117275. https://doi.org/10.1016/j.neuroimage.2020.117275
- Vahid, Amirali, et al. (2020). "Applying deep learning to single-trial EEG data provides evidence for complementary theories on action control." Communications biology 3.1 (2020): 1-11. https://doi.org/10.1038/s42003-020-0846-z
- Giller, Franziska, et al. (2020). "Evidence for a causal role of superior frontal cortex theta oscillations during the processing of joint subliminal and conscious conflicts." Cortex 132 (2020): 15-28. https://doi.org/10.1016/j.cortex.2020.08.003
- Pscherer, Charlotte, et al. (2019). "On the relevance of EEG resting theta activity for the neurophysiological dynamics underlying motor inhibitory control." Human brain mapping 40.14 (2019): 4253-4265. https://doi.org/10.1002/hbm.24699
- Wolff, Nicole, et al. (2019). "Paradoxical response inhibition advantages in adolescent obsessive compulsive disorder result from the interplay of automatic and controlled processes." NeuroImage: Clinical 23 (2019): 101893. https://doi.org/10.1016/j.nicl.2019.101893
- Schreiter, Marie Luise, et al. (2019). "How non-veridical perception drives actions in healthy humans: evidence from synaesthesia." Philosophical Transactions of the Royal Society B 374.1787 (2019): 20180574. https://doi.org/10.1098/rstb.2018.0574
- Tunc, Sinem, et al. (2019). "Predictive coding and adaptive behavior in patients with genetically determined cerebellar ataxia––A neurophysiology study." NeuroImage: Clinical 24 (2019): 102043. https://doi.org/10.1016/j.nicl.2019.102043
- Bensmann, Wiebke, et al. (2019). "The presynaptic regulation of dopamine and norepinephrine synthesis has dissociable effects on different kinds of cognitive conflicts." Molecular neurobiology 56.12 (2019): 8087-8100. https://doi.org/10.1007/s12035-019-01664-z
- Zink, Nicolas, et al. (2019). "The role of DRD1 and DRD2 receptors for response selection under varying complexity levels: Implications for metacontrol processes." International Journal of Neuropsychopharmacology 22.12: 747-753. https://doi.org/10.1093/ijnp/pyz024
- Bensmann, Wiebke, et al. (2020)."Dopamine D1, but not D2, signaling protects mental representations from distracting bottom-up influences." Neuroimage 204: 116243. . https://doi.org/10.1016/j.neuroimage.2019.116243
- Bensmann W, et al. (2019). Young frequent binge drinkers show no behavioral deficits in inhibitory control and cognitive flexibility. Prog Neuropsychopharmacol Biol Psychiatry 93: 93-101. doi: 10.1016/j.pnpbp.2019.03.019.
- Bensmann W, et al. (2019). Neuronal networks underlying the conjoint modulation of response selection by subliminal and consciously induced cognitive conflicts. Brain Struct Funct. doi: 10.1007/s00429-019-01866-0.
- Chmielewski W & Beste C (2019). Neurophysiological mechanisms underlying the modulation of cognitive control by simultaneous conflicts. Cortex 115:216-230. doi: 10.1016/j.cortex.2019.02.006.
- Bensmann W, et al. (2019). The Intensity of Early Attentional Processing, but Not Conflict Monitoring, Determines the Size of Subliminal Response Conflicts. Front Hum Neurosci 13: 53. doi: 10.3389/fnhum.2019.00053.
- Bensmann W, et al. (2019). Catecholaminergic effects on inhibitory control depend on the interplay of prior task experience and working memory demands. J Psychopharmacol. doi: 10.1177/0269881119827815.
- Zink N, et al. (2019). CHRM2 Genotype Affects Inhibitory Control Mechanisms During Cognitive Flexibility. Mol Neurobiol. doi: 10.1007/s12035-019-1521-6.
- Adelhöfer N, et al. (2019). Anodal tDCS affects neuromodulatory effects of the norepinephrine system on superior frontal theta activity during response inhibition. Brain Struct Funct. doi: 10.1007/s00429-019-01839-3.
- Chmielewski WX, et al. (2018). How high-dose alcohol intoxication affects the interplay of automatic and controlled processes. Addict Biol. doi: 10.1111/adb.12700.
- Friedrich J & Beste C (2018). Paradoxical, causal effects of sensory gain modulation on motor inhibitory control - a tDCS, EEG-source localization study. Sci Rep 8(1): 17486. doi: 10.1038/s41598-018-35879-2.
- Zink N, et al. (2018). On the Neurophysiological Mechanisms Underlying the Adaptability to Varying Cognitive Control Demands. Front Hum Neurosci 12: 411. doi: 10.3389/fnhum.2018.00411.
- Vahid A, et al. (2018). Machine learning provides novel neurophysiological features that predict performance to inhibit automated responses. Sci Rep 8(1): 16235. doi: 10.1038/s41598-018-34727-7.
- Beste C, et al. (2019). How minimal variations in neuronal cytoskeletal integrity modulate cognitive control. Neuroimage 185: 129-139. doi: 10.1016/j.neuroimage.2018.10.053.
- Zink N, et al. (2019). Apolipoprotein ε4 is associated with better cognitive control allocation in healthy young adults. Neuroimage 185: 274-285. doi: 10.1016/j.neuroimage.2018.10.046.
- Giller F, et al. (2018). The neurophysiological basis of developmental changes during sequential cognitive flexibility between adolescents and adults. Hum Brain Mapp. doi: 10.1002/hbm.24394.
- Zink N, et al. (2018). Detrimental effects of a high-dose alcohol intoxication on sequential cognitive flexibility are attenuated by practice. Prog Neuropsychopharmacol Biol Psychiatry 89:97-108. doi: 10.1016/j.pnpbp.2018.08.034.
- Zink N, et al. (2018). Alcohol Hangover Increases Conflict Load via Faster Processing of Subliminal Information. Front Hum Neurosci 12:316. doi: 10.3389/fnhum.2018.00316.
- Beste C, et al. (2018). Striatal Microstructure and Its Relevance for Cognitive Control. Trends Cogn Sci 22(9): 747-751. doi: 10.1016/j.tics.2018.06.007.
- Bensmann W, et al. (2018). Catecholaminergic Modulation of Conflict Control Depends on the Source of Conflicts. Int J Neuropsychopharmacol 21(10): 901-909. doi: 10.1093/ijnp/pyy063.
- Chmielewski WX, et al. (2018). Effects of multisensory stimuli on inhibitory control in adolescent ADHD: It is the content of information that matters. Neuroimage Clin 19:527-537. doi: 10.1016/j.nicl.2018.05.019.
- Stock AK, et al. (2018). On the effects of tyrosine supplementation on interference control in a randomized, double-blind placebo-control trial. Eur Neuropsychopharmacol 28(8):933-944. doi: 10.1016/j.euroneuro.2018.05.010.
- Stock AK, et al. (2019). Methamphetamine-associated difficulties in cognitive control allocation may normalize after prolonged abstinence. Prog Neuropsychopharmacol Biol Psychiatry 88:41-52. doi: 10.1016/j.pnpbp.2018.06.015.
- Zink N, et al. (2018). Evidence for a neuronal dual-process account for adverse effects of cognitive control. Brain Struct Funct 223(7):3347-3363. doi: 10.1007/s00429-018-1694-1.
- Schreiter ML, et al. (2018). How socioemotional setting modulates late-stage conflict resolution processes in the lateral prefrontal cortex. Cogn Affect Behav Neurosci 18:521–535. doi: 10.3758/s13415-018-0585-5.
- Petruo VA, et al. (2018). On the role of the prefrontal cortex in fatigue effects on cognitive flexibility - a system neurophysiological approach. Sci Rep 8:6395. doi: 10.1038/s41598-018-24834-w.
- Wolff N, et al. (2018). When repetitive mental sets increase cognitive flexibility in adolescent obsessive-compulsive disorder. J Child Psychol Psychiatry. doi: 10.1111/jcpp.12901.
- Schreiter ML, et al. (2018). Neurophysiological processes and functional neuroanatomical structures underlying proactive effects of emotional conflicts. NeuroImage 174:11–21. doi: 10.1016/j.neuroimage.2018.03.017.
- Chmielewski WX, et al. (2018). Response selection codes in neurophysiological data predict conjoint effects of controlled and automatic processes during response inhibition. Hum Brain Mapp 39:1839–1849. doi: 10.1002/hbm.23974.
- Bodmer B, et al. (2018). Neurophysiological variability masks differences in functional neuroanatomical networks and their effectiveness to modulate response inhibition between children and adults. Brain Struct Funct 223:1797–1810. doi: 10.1007/s00429-017-1589-6.
- Petruo VA, et al. (2017). Specific neurophysiological mechanisms underlie cognitive inflexibility in inflammatory bowel disease. Sci Rep 7:13943. doi: 10.1038/s41598-017-14345-5.
- Wolff N, et al. (2017). On the relevance of the alpha frequency oscillation’s small-world network architecture for cognitive flexibility. Sci Rep 7:13910. doi: 10.1038/s41598-017-14490-x.
- Zhang R, et al. (2017). Self-Regulatory Capacities Are Depleted in a Domain-Specific Manner. Front Syst Neurosci 11:70. doi: 10.3389/fnsys.2017.00070.
- Wolff N, et al. (2017). The role of phasic norepinephrine modulations during task switching: evidence for specific effects in parietal areas. Brain Struct Funct 223(2):925-940. doi: 10.1007/s00429-017-1531-y.
- Letzner S, et al. (2017). How birds outperform humans in multi-component behavior. Curr Biol 27:R996–R998. doi: 10.1016/j.cub.2017.07.056.
- Friedrich J, et al. (2018). Specific properties of the SI and SII somatosensory areas and their effects on motor control: a system neurophysiological study. Brain Struct Funct 223:687–699. doi: 10.1007/s00429-017-1515-y.
- Stock AK, et al. (2017). Opposite effects of binge drinking on consciously vs. subliminally induced cognitive conflicts. NeuroImage 162:117–126. doi: 10.1016/j.neuroimage.2017.08.066.
- Stock AK, et al. (2017). Humans with latent toxoplasmosis display altered reward modulation of cognitive control. Sci Rep 7:10170. doi: 10.1038/s41598-017-10926-6.
- Mückschel M, et al. (2017). Distinguishing stimulus and response codes in theta oscillations in prefrontal areas during inhibitory control of automated responses. Hum Brain Mapp 38:5681–5690. doi: 10.1002/hbm.23757.
- Bluschke A, et al. (2017). Neuronal Intra-Individual Variability Masks Response Selection Differences between ADHD Subtypes-A Need to Change Perspectives. Front Hum Neurosci 11:329. doi: 10.3389/fnhum.2017.00329.
- Stock AK, et al. (2017). On the effects of multimodal information integration in multitasking. Sci Rep 7:4927. doi: 10.1038/s41598-017-04828-w.
- Friedrich J, et al. (2017). Somatosensory lateral inhibition processes modulate motor response inhibition - an EEG source localization study. Sci Rep 7:4454. doi: 10.1038/s41598-017-04887-z.
- Gohil K, et al. (2017). Sensory processes modulate differences in multi-component behavior and cognitive control between childhood and adulthood. Hum Brain Mapp 38(10):4933-4945. doi: 10.1002/hbm.23705.
- Dippel G, et al. (2017). Demands on response inhibition processes determine modulations of theta band activity in superior frontal areas and correlations with pupillometry - Implications for the norepinephrine system during inhibitory control. NeuroImage 157:575–585. doi: 10.1016/j.neuroimage.2017.06.037.
- Beste C, et al. (2017). The Basal Ganglia Striosomes Affect the Modulation of Conflicts by Subliminal Information-Evidence from X-Linked Dystonia Parkinsonism. Cereb Cortex 28(7):2243-2252. doi: 10.1093/cercor/bhx125.
- Wolff N, et al. (2017). Neural mechanisms and functional neuroanatomical networks during memory and cue-based task switching as revealed by residue iteration decomposition (RIDE) based source localization. Brain Struct Funct 222(8):3819-3831. doi: 10.1007/s00429-017-1437-8.
- Beste C, et al. (2017). Dysfunctions in striatal microstructure can enhance perceptual decision making through deficits in predictive coding. Brain Struct Funct 222(8):3807-3817. doi: 10.1007/s00429-017-1435-x.
- Colzato LS, et al. (2017). Darwin revisited: The vagus nerve is a causal element in controlling recognition of other’s emotions. Cortex 92:95–102. doi: 10.1016/j.cortex.2017.03.017.
- Wolff N, et al. (2017). Modulations of cognitive flexibility in obsessive compulsive disorder reflect dysfunctions of perceptual categorization. J Child Psychol Psychiatry 58(8):939-949. doi: 10.1111/jcpp.12733.
- Stock AK, Beste C (2017). On the necessity of translational cognitive-neurotoxicological research in methamphetamine abuse and addiction. Arch Toxicol 91(7):2707-2709. doi: 10.1007/s00204-017-1972-3.
- Stock AK (2017). Barking up the Wrong Tree: Why and How We May Need to Revise Alcohol Addiction Therapy. Front Psychol 8:884. doi: 10.3389/fpsyg.2017.00884.
- Gohil K, et al. (2017). ADHD patients fail to maintain task goals in face of subliminally and consciously induced cognitive conflicts. Psychol Med 47(10):1771-1783. doi: 10.1017/S0033291717000216.
- Wolff N, et al. (2017). Working memory load affects repetitive behaviour but not cognitive flexibility in adolescent autism spectrum disorder. World J Biol Psychiatry. doi: 10.1080/15622975.2017.
- Mückschel M, et al. (2017). The norepinephrine system shows information-content specific properties during cognitive control - Evidence from EEG and pupillary responses. NeuroImage 149:44–52. doi: 10.1016/j.neuroimage.2017.01.036.
- Beste C, et al. (2017). Striosomal dysfunction affects behavioral adaptation but not impulsivity-Evidence from X-linked dystonia-parkinsonism. Mov Disord 32(4): 576–584. doi: 10.1002/mds.26895.
- Bodmer B, Beste C (2017). On the dependence of response inhibition processes on sensory modality. Hum Brain Mapp 38(4):1941–1951. doi: 10.1002/hbm.23495.
- Stock AK, et al. (2016). Subliminally and consciously induced cognitive conflicts interact at several processing levels. Cortex 85:75–89. doi: 10.1016/j.cortex.2016.09.027.
- Wolff N, et al. (2016). Effects of high-dose ethanol intoxication and hangover on cognitive flexibility. Addict Biol 23(1):503-514. doi: 10.1111/adb.12470
- Chmielewski WX, Beste C (2017). Testing interactive effects of automatic and conflict control processes during response inhibition - A system neurophysiological study. NeuroImage 146:1149–1156. doi: 10.1016/j.neuroimage.2016.10.015.
- Mückschel M, et al. (2017). The norepinephrine system and its relevance for multi-component behavior. NeuroImage 146:1062–1070. doi: 10.1016/j.neuroimage.2016.10.007.
- Beste C, et al. (2016). Effects of Concomitant Stimulation of the GABAergic and Norepinephrine System on Inhibitory Control - A Study Using Transcutaneous Vagus Nerve Stimulation. Brain Stimul 9(6):811-818. doi: 10.1016/j.brs.2016.07.004.
- Chmielewski WX, et al. (2017). The norepinephrine system affects specific neurophysiological subprocesses in the modulation of inhibitory control by working memory demands. Hum Brain Mapp 38(1):68–81. doi: 10.1002/hbm.23344.
- Stock AK, et al. (2016). The system neurophysiological basis of non-adaptive cognitive control: Inhibition of implicit learning mediated by right prefrontal regions. Hum Brain Mapp 37(12):4511-4522. doi: 10.1002/hbm.23325.
- Colzato LS, et al. (2016). Effects of l-Tyrosine on working memory and inhibitory control are determined by DRD2 genotypes: A randomized controlled trial. Cortex 82:217–224. doi: 10.1016/j.cortex.2016.06.010.