Sensory inputs, neuromodulators and control

A year in research · 28 selected publications · five research threads

In 2017, we traced cognitive control back to the sensory codes, bodily signals and neuromodulatory systems that prepare an action.

The studies showed that inhibition and multitasking are shaped before the final response: by modality, multimodal integration, prediction, working memory and norepinephrine-related preparation.

01 · INFORMATION CODES

Control networks represent different things

Theta oscillations in prefrontal cortex carried separable stimulus and response codes during the inhibition of automatic actions.[1] Pupil-linked and EEG measures showed that norepinephrine-related activity was strongest for motor-response information and prepared control when inhibition was unlikely or multi-component demands might arise.[2,3,4] Working-memory load recruited norepinephrine-sensitive right frontal processes during stopping.[5]

Blocking, usually studied in conditioning, also changed medial-frontal response selection in goal-directed behaviour.[6] Automatic response tendencies could paradoxically make stopping more accurate by increasing cingulate conflict monitoring.[7]

In plain terms: The brain does not broadcast one generic control signal; it represents stimuli, decisions and motor responses with partly distinct dynamics.

02 · SENSORY FOUNDATIONS

The route into the system changes the system

The network supporting response inhibition depended on whether information arrived through vision or audition.[8] Somatosensory lateral inhibition affected later motor stopping, especially when information had to cross hemispheres.[9] Multimodal integration changed multitasking through premotor and visual-association regions, and helped explain developmental differences between children and adults.[10,11]

These findings were not confined to the laboratory. Changing proprioceptive information reversed some effects of alcohol on response control, while circadian impairment in restless legs syndrome arose from early visual selection rather than later conflict monitoring.[12,13]

In plain terms: Executive performance cannot be understood independently of the sensory and bodily information on which it operates.

03 · FLEXIBLE TASK SETS

Updating internal rules is a distinct operation

Temporal decomposition localized memory- and cue-based switching differences to updating internal response-selection representations in inferior parietal cortex.[14] More efficient reactive switching was associated with a more small-world-like alpha network.[15] In OCD, extra working-memory demand exposed difficulties in perceptual categorization and task-set updating.[16] In inflammatory bowel disease, similar behavioural inflexibility reflected overtaxed neural circuits.[17]

A neurotoxicology translation study found that manganese-exposed welders did not show impaired flexibility or multitasking despite differences in an EEG marker.[18] That negative result underscored why behaviour and physiology must be interpreted together.

In plain terms: Switching depends on updating an internal task representation, and physiological differences do not automatically imply functional impairment.

04 · CLINICAL MECHANISMS

Similar symptoms, different neural routes

ADHD was marked by weak shielding of task goals against both conscious and subliminal conflict; accounting for intra-individual variability also revealed differences between inattentive and combined presentations.[19,20] ADD and neurofibromatosis type 1 could look clinically similar while showing different inhibitory physiology, and NF1 used a different route to successful conflict performance.[21,22]

Tourette syndrome showed enhanced integration in multi-component behaviour, possibly related to long-term tic control or frontostriatal connectivity.[23] Striosomal dysfunction in X-linked dystonia-parkinsonism unexpectedly improved perceptual decisions under distraction by reducing predictive interference.[24]

In plain terms: Behavioural resemblance is not mechanistic identity; distinct neural strategies can lead to the same score or symptom.

05 · STATE AND INTERVENTION

Biological state can reverse an effect

Binge-like intoxication reduced the efficiency of evidence accumulation, yet the following hangover increased it.[25] Alcohol also increased consciously perceived conflict while reducing subliminal conflict, indicating less attention to weak signals rather than a unitary control deficit.[26] Reward processing in latent toxoplasmosis was altered through additional resource allocation.[27]

Transcutaneous vagus nerve stimulation causally improved recognition of easily decoded facial emotions, linking bodily neuromodulation to social perception.[28] Together these studies showed that the direction of an effect depends on task content, salience and current physiological state.

In plain terms: The same biological manipulation can help one operation and harm another, so mechanism and context must be specified together.

What 2017 added up to

The 2017 work placed sensory coding and neuromodulatory preparation at the heart of action control. It also demonstrated why clinical and state effects must be localized within a processing cascade instead of summarized as globally better or worse control.

Selected publications

Curated from PubMed records returned for Beste C[au] in 2017. Citation numbers in the story link to entries below. DOI links open the publisher landing page; PubMed links open the indexed record.

1. Distinguishing stimulus and response codes in theta oscillations in prefrontal areas during inhibitory control of automated responses.

Mückschel M, Dippel G, Beste C. Human brain mapping. 2017;38(11):5681-5690.

DOI: 10.1002/hbm.23757   ·   PubMed

2. The norepinephrine system shows information-content specific properties during cognitive control - Evidence from EEG and pupillary responses.

Mückschel M, Chmielewski W, Ziemssen T, Beste C. NeuroImage. 2017;149:44-52.

DOI: 10.1016/j.neuroimage.2017.01.036   ·   PubMed

3. 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.

Dippel G, Mückschel M, Ziemssen T, Beste C. NeuroImage. 2017;157:575-585.

DOI: 10.1016/j.neuroimage.2017.06.037   ·   PubMed

4. The norepinephrine system and its relevance for multi-component behavior.

Mückschel M, Gohil K, Ziemssen T, Beste C. NeuroImage. 2017;146:1062-1070.

DOI: 10.1016/j.neuroimage.2016.10.007   ·   PubMed

5. The norepinephrine system affects specific neurophysiological subprocesses in the modulation of inhibitory control by working memory demands.

Chmielewski WX, Mückschel M, Ziemssen T, Beste C. Human brain mapping. 2017;38(1):68-81.

DOI: 10.1002/hbm.23344   ·   PubMed

6. Blocking effects in non-conditioned goal-directed behaviour.

Stock AK, Gohil K, Beste C. Brain structure & function. 2017;222(6):2807-2818.

DOI: 10.1007/s00429-017-1373-7   ·   PubMed

7. Testing interactive effects of automatic and conflict control processes during response inhibition - A system neurophysiological study.

Chmielewski WX, Beste C. NeuroImage. 2017;146:1149-1156.

DOI: 10.1016/j.neuroimage.2016.10.015   ·   PubMed

8. On the dependence of response inhibition processes on sensory modality.

Bodmer B, Beste C. Human brain mapping. 2017;38(4):1941-1951.

DOI: 10.1002/hbm.23495   ·   PubMed

9. Somatosensory lateral inhibition processes modulate motor response inhibition - an EEG source localization study.

Friedrich J, Mückschel M, Beste C. Scientific reports. 2017;7(1):4454.

DOI: 10.1038/s41598-017-04887-z   ·   PubMed

10. On the effects of multimodal information integration in multitasking.

Stock AK, Gohil K, Huster RJ, Beste C. Scientific reports. 2017;7(1):4927.

DOI: 10.1038/s41598-017-04828-w   ·   PubMed

11. Sensory processes modulate differences in multi-component behavior and cognitive control between childhood and adulthood.

Gohil K, Bluschke A, Roessner V, Stock AK, Beste C. Human brain mapping. 2017;38(10):4933-4945.

DOI: 10.1002/hbm.23705   ·   PubMed

12. Reversal of alcohol-induced effects on response control due to changes in proprioceptive information processing.

Stock AK, Mückschel M, Beste C. Addiction biology. 2017;22(1):246-256.

DOI: 10.1111/adb.12296   ·   PubMed

13. Neurophysiological mechanisms of circadian cognitive control in RLS patients - an EEG source localization study.

Zhang R, Brandt MD, Schrempf W, Beste C, Stock AK. NeuroImage. Clinical. 2017;15:644-652.

DOI: 10.1016/j.nicl.2017.06.018   ·   PubMed

14. Neural mechanisms and functional neuroanatomical networks during memory and cue-based task switching as revealed by residue iteration decomposition (RIDE) based source localization.

Wolff N, Mückschel M, Beste C. Brain structure & function. 2017;222(8):3819-3831.

DOI: 10.1007/s00429-017-1437-8   ·   PubMed

15. On the relevance of the alpha frequency oscillation's small-world network architecture for cognitive flexibility.

Wolff N, Zink N, Stock AK, Beste C. Scientific reports. 2017;7(1):13910.

DOI: 10.1038/s41598-017-14490-x   ·   PubMed

16. Modulations of cognitive flexibility in obsessive compulsive disorder reflect dysfunctions of perceptual categorization.

Wolff N, Buse J, Tost J, Roessner V, Beste C. Journal of child psychology and psychiatry, and allied disciplines. 2017;58(8):939-949.

DOI: 10.1111/jcpp.12733   ·   PubMed

17. Specific neurophysiological mechanisms underlie cognitive inflexibility in inflammatory bowel disease.

Petruo VA, Zeißig S, Schmelz R, Hampe J, Beste C. Scientific reports. 2017;7(1):13943.

DOI: 10.1038/s41598-017-14345-5   ·   PubMed

18. Are multitasking abilities impaired in welders exposed to manganese? Translating cognitive neuroscience to neurotoxicology.

van Thriel C, Quetscher C, Pesch B, Lotz A, et al.. Archives of toxicology. 2017;91(8):2865-2877.

DOI: 10.1007/s00204-017-1932-y   ·   PubMed

19. ADHD patients fail to maintain task goals in face of subliminally and consciously induced cognitive conflicts.

Gohil K, Bluschke A, Roessner V, Stock AK, Beste C. Psychological medicine. 2017;47(10):1771-1783.

DOI: 10.1017/S0033291717000216   ·   PubMed

20. Neuronal Intra-Individual Variability Masks Response Selection Differences between ADHD Subtypes-A Need to Change Perspectives.

Bluschke A, Chmielewski WX, Mückschel M, Roessner V, Beste C. Frontiers in human neuroscience. 2017;11:329.

DOI: 10.3389/fnhum.2017.00329   ·   PubMed

21. Response inhibition in Attention deficit disorder and neurofibromatosis type 1 - clinically similar, neurophysiologically different.

Bluschke A, von der Hagen M, Papenhagen K, Roessner V, Beste C. Scientific reports. 2017;7:43929.

DOI: 10.1038/srep43929   ·   PubMed

22. Conflict processing in juvenile patients with neurofibromatosis type 1 (NF1) and healthy controls - Two pathways to success.

Bluschke A, von der Hagen M, Papenhagen K, Roessner V, Beste C. NeuroImage. Clinical. 2017;14:499-505.

DOI: 10.1016/j.nicl.2017.02.014   ·   PubMed

23. Evidence for enhanced multi-component behaviour in Tourette syndrome - an EEG study.

Brandt VC, Stock AK, Münchau A, Beste C. Scientific reports. 2017;7(1):7722.

DOI: 10.1038/s41598-017-08158-9   ·   PubMed

24. Dysfunctions in striatal microstructure can enhance perceptual decision making through deficits in predictive coding.

Beste C, Mückschel M, Rosales R, Domingo A, et al.. Brain structure & function. 2017;222(8):3807-3817.

DOI: 10.1007/s00429-017-1435-x   ·   PubMed

25. Effects of binge drinking and hangover on response selection sub-processes-a study using EEG and drift diffusion modeling.

Stock AK, Hoffmann S, Beste C. Addiction biology. 2017;22(5):1355-1365.

DOI: 10.1111/adb.12412   ·   PubMed

26. Opposite effects of binge drinking on consciously vs. subliminally induced cognitive conflicts.

Stock AK, Wolff N, Beste C. NeuroImage. 2017;162:117-126.

DOI: 10.1016/j.neuroimage.2017.08.066   ·   PubMed

27. Humans with latent toxoplasmosis display altered reward modulation of cognitive control.

Stock AK, Dajkic D, Köhling HL, von Heinegg EH, Fiedler M, Beste C. Scientific reports. 2017;7(1):10170.

DOI: 10.1038/s41598-017-10926-6   ·   PubMed

28. Darwin revisited: The vagus nerve is a causal element in controlling recognition of other's emotions.

Colzato LS, Sellaro R, Beste C. Cortex; a journal devoted to the study of the nervous system and behavior. 2017;92:95-102.

DOI: 10.1016/j.cortex.2017.03.017   ·   PubMed