Catecholaminergic manipulation alters dynamic network topology across cognitive states

Network Neuroscience

Volumn 2, Issue 3, 2018, Pages 381-396

  Shine, James M ^a,b   van den Brink, Ruud L ^c   Hernaus, Dennis ^d   Nieuwenhuis, Sander ^c   Poldrack, Russell A ^a  

^a STANFORD UNIVERSITY   (United States)

^b UNIVERSITY OF SYDNEY   (Australia)

^c LEIDEN UNIVERSITY   (Netherlands)

^d UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

Author keywords

Atomoxetine; Flexibility; fMRI; Integration; Network; Noradrenaline

Indexed keywords

ATOMOXETINE; CATECHOLAMINE; PLACEBO;

ADULT; ARTICLE; BRAIN FUNCTION; CATECHOLAMINE BLOOD LEVEL; COGNITION; CONNECTOME; CONTROLLED STUDY; CROSSOVER PROCEDURE; DOUBLE BLIND PROCEDURE; FEMALE; FUNCTIONAL CONNECTIVITY; FUNCTIONAL MAGNETIC RESONANCE IMAGING; FUNCTIONAL NEUROIMAGING; HUMAN; LOCUS CERULEUS; MALE; NORMAL HUMAN; RANDOMIZED CONTROLLED TRIAL; SINGLE DRUG DOSE;

EID: 85077174748     PISSN: None     EISSN: 24721751     Source Type: Journal    
DOI: 10.1162/netn_a_00042     Document Type: Article

References (60)

1. Aston-Jones, G., & Cohen, J. D. (2005). An integrative theory of locus coeruleus-norepinephrine function: Adaptive gain and optimal performance. Annual Review of Neuroscience, 28(1), 403–450.
2. Bari, A., & Aston-Jones, G. (2013). Atomoxetine modulates spontaneous and sensory-evoked discharge of locus coeruleus noradrenergic neurons. Neuropharmacology, 64, 53–64.
3. Bassett, D. S., Yang, M., Wymbs, N. F., & Grafton, S. T. (2015). Learning-induced autonomy of sensorimotor systems. Nature Neuroscience, 18(5), 744–751. https://doi.org/10.1038/nn.3993
4. Bayer, A. (2016). Applied statistics analysis of variance and regression. Applied Statistics.
5. Behzadi, Y., Restom, K., Liau, J., & Liu, T. T. (2007). A component based noise correction method (CompCor) for BOLD and perfusion based fMRI. NeuroImage, 37(1), 90–101.
6. Berridge, C. W., & Waterhouse, B. D. (2003). The locus coeruleus–noradrenergic system: Modulation of behavioral state and state-dependent cognitive processes. Brain Research Reviews, 42(1), 33–84.
7. Bullmore, E., & Sporns, O. (2012). The economy of brain network organization. Nature Reviews Neuroscience, 13(5), 336–349.
8. Carter, M. E., Yizhar, O., Chikahisa, S., Nguyen, H., Adamantidis, A., Nishino, S., (2010). Tuning arousal with optogenetic modulation of locus coeruleus neurons. Nature Neuroscience, 13(12), 1526–1533.
9. Chen, N., & Reith, M. (2000). Structure and function of the dopamine transporter. European Journal of Pharmacology, 405, 329–339.
10. Cole, M. W., Reynolds, J. R., Power, J. D., Repovs, G., Anticevic, A., & Braver, T. S. (2013). Multi-task connectivity reveals flexible hubs for adaptive task control. Nature Neuroscience, 16(9), 1348–1355.
11. Cools, R., & D’Esposito, M. (2011). Inverted-U-shaped dopamine actions on human working memory and cognitive control. Biological Psychiatry, 69(12), e113–e125.
12. de Pasquale, F., Penna, Della S., Sporns, O., Romani, G. L., & Corbetta, M. (2016). A dynamic core network and global efficiency in the resting human brain. Cerebral Cortex, 26(10), 4015–4033.
13. Devilbiss, D. M., & Waterhouse, B. D. (2011). Phasic and tonic patterns of locus coeruleus output differentially modulate sensory network function in the awake rat. Journal of Neurophysiology, 105(1), 69–87.
14. 2-adrenoceptor mediated co-release of dopamine and noradrenaline from noradrenergic neurons in the cerebral cortex. Journal of Neuroscience, 88, 1003–1009.
15. Diedrichsen, J., Balsters, J. H., Flavell, J., Cussans, E., & Ramnani, N. (2009). A probabilistic MR atlas of the human cerebellum. NeuroImage, 46(1), 39–46.
16. Ding, Y. S., Naganawa, M., Gallezot, J.-D., Nabulsi, N., Lin, S.-F., Ropchan, J., (2014). Clinical doses of atomoxetine significantly occupy both norepinephrine and serotonin transports: Implications on treatment of depression and ADHD. NeuroImage, 86, 164–171.
17. Eldar, E., Cohen, J. D., & Niv, Y. (2013). The effects of neural gain on attention and learning. Nature Neuroscience, 16(8), 1146–1153.
18. Gordon, E. M., Laumann, T. O., Adeyemo, B., Huckins, J. F., Kelley, W. M., & Petersen, S. E. (2014). Generation and evaluation of a cortical area parcellation from resting-state correlations. Cerebral Cortex, bhu239.
19. Guimerà, R., & Nunes Amaral, L. A. (2005). Functional cartography of complex metabolic networks. Nature, 433(7028), 895–900.
20. Hermans, E. J., van Marle, H., & Ossewaarde, L. (2011). Stress-related noradrenergic activity prompts large-scale neural network reconfiguration. Science, 334, 1151–1153.
21. Hernaus, D., Casales Santa, M. M., Offermann, J. S., & Van Amelsvoort, T. (2017). Noradrenaline transporter blockade increases fronto-parietal functional connectivity relevant for working memory. European Neuropsychopharmacology, 27(4), 399–410.
22. Hutchison, R. M., Womelsdorf, T., Allen, E. A., Bandettini, P. A., Calhoun, V. D., Corbetta, M., (2013). Dynamic functional connectivity: Promise, issues, and interpretations. NeuroImage, 80, 360–378.
23. Invernizzi, R. W., & Garattini, S. (2004). Role of presynaptic α2-adrenoceptors in antidepressant action: recent findings from microdialysis studies. Progress in Neuro-Psychopharmacology and Biological Psychiatry, 28(5), 819–827.
24. Joshi, S., Li, Y., Kalwani, R. M., & Gold, J. I. (2016). Relationships between pupil diameter and neuronal activity in the locus coeruleus, colliculi, and cingulate cortex. Neuron, 89(1), 221–234.
25. Kitzbichler, M. G., Henson, R. N. A., Smith, M. L., Nathan, P. J., & Bullmore, E. T. (2011). Cognitive effort drives workspace configuration of human brain functional networks. The Journal of Neuroscience, 31(22), 8259–8270.
26. Kuhn, H. W. (1955). The Hungarian method for the assignment problem. Naval Research Logistics, 2(1), 83–97.
27. Laumann, T. O., Snyder, A. Z., Mitra, A., & Gordon, E. M. (2016). On the stability of bold fmri correlations. Cerebral Cortex, 27(10), 4719–4732.
28. Liégeois, R., Laumann, T. O., Snyder, A. Z., Zhou, J., & Yeo, B. T. T. (2017). Interpreting temporal fluctuations in resting-state functional connectivity MRI. NeuroImage, 163, 437–455.
29. Liu, L.-L., Yang, J., Lei, G.-F., Wang, G.-J., Wang, Y.-W., & Sun, R.-P. (2008). Atomoxetine increases histamine release and improves learning deficits in an animal model of attention-deficit hyperactivity disorder: the spontaneously hypertensive rat. Basic & Clinical Pharmacology & Toxicology, 102(6), 527–532.
30. Mattar, M. G., Cole, M. W., Thompson-Schill, S. L., & Bassett, D. S. (2015). A functional cartography of cognitive systems. PLoS Computational Biology, 11(12), e1004533.
31. McGinley, M. J., David, S. V., & McCormick, D. A. (2015a). Cortical membrane potential signature of optimal states for sensory signal detection. Neuron, 87(1), 179–192.
32. McGinley, M. J., Vinck, M., Reimer, J., Batista-Brito, R., Zagha, E., Cadwell, C. R., (2015b). Waking state: Rapid variations modulate neural and behavioral responses. Neuron, 87(6), 1143–1161.
33. Medaglia, J. D., Lynall, M. E., & Bassett, D. S. (2015). Cognitive network neuroscience. Journal of Cognitive Neuroscience, 27(8), 1471–1491.
34. Miller, R. L., Adali, J., Levin-Schwarz, Y., & Calhoun, V. D. (2017). Resting-state fMRI dynamics and null models: Perspectives, sampling variability, and simulations. biorxiv.
35. Morón, J. A., Brockington, A., & Wise, R. A. (2002). Dopamine uptake through the norepinephrine transporter in brain regions with low levels of the dopamine transporter: Evidence from knock-out mouse lines. Journal of Neuroscience, 22, 389–395.
36. Mucha, P. J., Richardson, T., Macon, K., Porter, M. A., & Onnela, J.-P. (2010). Community structure in time-dependent, multiscale, and multiplex networks. Science, 328(5980), 876–878.
37. Nichols, T. E., & Holmes, A. P. (2002). Nonparametric permutation tests for functional neuroimaging: a primer with examples. Human Brain Mapping, 15(1), 1–25.
38. Nieuwenhuis, S., De Geus, E. J., & Aston-Jones, G. (2011). The anatomical and functional relationship between the P3 and autonomic components of the orienting response. Psychophysiology, 48(2), 162–175.
39. Power, J. D., Mitra, A., Laumann, T. O., Snyder, A. Z., Schlaggar, B. L., & Petersen, S. E. (2014). Methods to detect, characterize, and remove motion artifact in resting state fMRI. NeuroImage, 84, 320–341.
40. Reimer, J., Froudarakis, E., Cadwell, C. R., Yatsenko, D., Denfield, G. H., & Tolias, A. S. (2014). Pupil fluctuations track fast switching of cortical states during quiet wakefulness. Neuron, 84(2), 355–362.
41. Reimer, J., McGinley, M. J., Liu, Y., Rodenkirch, C., Wang, Q., McCormick, D. A., & Tolias, A. S. (2016). Pupil fluctuations track rapid changes in adrenergic and cholinergic activity in cortex. Nature Communications, 7, 13289.
42. Robbins, T. W., & Arnsten, A. F. T. (2009). The neuropsychopharmacology of fronto-executive function: Monoaminergic modulation. Annual Review of Neuroscience, 32(1), 267–287.
43. Rubinov, M., & Sporns, O. (2010). Complex network measures of brain connectivity: Uses and interpretations. NeuroImage, 52(3), 1059–1069.
44. Safaai, H., Neves, R., Eschenko, O., Logothetis, N. K., & Panzeri, S. (2015). Modeling the effect of locus coeruleus firing on cortical state dynamics and single-trial sensory processing. Proceedings of the National Academy of Sciences of the United States of America, 112(41), 12834–12839.
45. Sakoğlu, U., Pearlson, G. D., Kiehl, K. A., Wang, Y. M., Michael, A. M., & Calhoun, V. D. (2010). A method for evaluating dynamic functional network connectivity and task-modulation: application to schizophrenia. Magma (New York, N.Y.), 23(5-6), 351–366.
46. Salimi-Khorshidi, G., Douaud, G., & Beckmann, C. F. (2014). Automatic denoising of functional MRI data: Combining independent component analysis and hierarchical fusion of classifiers. NeuroImage, 90, 449–468.
47. Samuels, E. R., & Szabadi, E. (2008). Functional neuroanatomy of the noradrenergic locus coeruleus: Its roles in the regulation of arousal and autonomic function Part II: Physiological and pharmacological manipulations and pathological alterations of locus coeruleus activity in humans. Current Neuropharmacology, 6(3), 254–285.
48. Sara, S. J. (2009). The locus coeruleus and noradrenergic modulation of cognition. Nature Reviews Neuroscience, 10(3), 211–223.
49. Sara, S. J., & Bouret, S. (2012). Orienting and reorienting: The locus coeruleus mediates cognition through arousal. Neuron, 76(1), 130–141.
50. Servan-Schreiber, D., Printz, H., & Cohen, J. (1990). A network model of catecholamine effects- gain, signal-to-noise ratio, and behavior. Science, 249, 892–895.
51. Shine, J. M., & Poldrack, R. A. (in press). Principles of dynamic network reconfiguration across diverse brain states. NeuroImage. Retrieved from https://www.sciencedirect.com/science/article/pii/s1053811917306572?via%3dihub
52. Shine, J. M., Aburn, M. J., Breakspear, M., & Poldrack, R. A. (in press). The modulation of neural gain facilitates a transition between functional segregation and integration in the brain. eLife. Retrieved from https://elifesciences.org/articles/31130
53. Shine, J. M., Bissett, P. G., Bell, P. T., Koyejo, O., Balsters, J. H., Gorgolewski, K. J., (2016). The dynamics of functional brain networks: Integrated network states during cognitive task performance. Neuron, 92(2), 544–554.
54. Shine, J. M., Koyejo, O., Bell, P. T., Gorgolewski, K. J., Gilat, M., & Poldrack, R. A. (2015). Estimation of dynamic functional connectivity using Multiplication of Temporal Derivatives. NeuroImage, 122, 399–407.
55. Shine, J. M., van den Brink, R. L., Hernaus, D., Nieuwenhuis, S., & Poldrack, R. A. (2018). Supporting Information for “Catecholaminergic manipulation alters dynamic network topology across cognitive states.” Network Neuroscience, 2(3), 381–396. https://doi.org/10.1162/netn_a_00042
56. Toussay, X., Basu, K., Lacoste, B., & Hamel, E. (2013). Locus coeruleus stimulation recruits a broad cortical neuronal network and increases cortical perfusion. The Journal of Neuroscience, 33(8), 3390–3401.
57. van den Brink, R. L., Pfeffer, T., Warren, C. M., Murphy, P. R., Tona, K.-D., van der Wee, N. J. A., (2016). Catecholaminergic neuromodulation shapes intrinsic MRI functional connectivity in the human brain. The Journal of Neuroscience, 36(30), 7865–7876.
58. Vatansever, D., Menon, D. K., Manktelow, A. E., Sahakian, B. J., & Stamatakis, E. A. (2015). Default mode dynamics for global functional integration. The Journal of Neuroscience, 35(46), 15254–15262.
59. Warren, C. M., van den Brink, R. L., Nieuwenhuis, S., & Bosch, J. A. (2017). Norepinephrine transporter blocker atomoxetine increases salivary alpha amylase. Psychoneuroendocrinology, 78, 233–236.
60. Waterhouse, B. D., Moises, H. C., & Woodward, D. J. (1980). Noradrenergic modulation of somatosensory cortical neuronal responses to lontophoretically applied putative neurotransmitters. Experimental Neurology, 69(1), 30–49.