Table of Contents Author Guidelines Submit a Manuscript
Neural Plasticity
Volume 2017, Article ID 4328015, 12 pages
https://doi.org/10.1155/2017/4328015
Review Article

Could LC-NE-Dependent Adjustment of Neural Gain Drive Functional Brain Network Reorganization?

1INSERM, U1028, CNRS UMR5292, Lyon Neuroscience Research Center, ImpAct Team, 69000 Lyon, France
2UCBL, 69000 Lyon, France

Correspondence should be addressed to Carole Guedj; rf.oohay@jdeugelorac and Fadila Hadj-Bouziane; rf.mresni@enaizuob-jdah.alidaf

Received 6 January 2017; Accepted 1 March 2017; Published 21 May 2017

Academic Editor: Oxana Eschenko

Copyright © 2017 Carole Guedj et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. G. Aston-Jones, J. Rajkowski, and J. Cohen, “Role of locus coeruleus in attention and behavioral flexibility,” Biological Psychiatry, vol. 46, no. 9, pp. 1309–1320, 1999. View at Publisher · View at Google Scholar · View at Scopus
  2. A. A. Kehagia, G. K. Murray, and T. W. Robbins, “Learning and cognitive flexibility: frontostriatal function and monoaminergic modulation,” Current Opinion in Neurobiology, vol. 20, no. 2, pp. 199–204, 2010. View at Publisher · View at Google Scholar · View at Scopus
  3. A. F. T. Arnsten, M. J. Wang, and C. D. Paspalas, “Neuromodulation of thought: flexibilities and vulnerabilities in prefrontal cortical network synapses,” Neuron, vol. 76, no. 1, pp. 223–239, 2012. View at Publisher · View at Google Scholar · View at Scopus
  4. S. J. Sara and S. Bouret, “Orienting and reorienting: the locus coeruleus mediates cognition through arousal,” Neuron, vol. 76, no. 1, pp. 130–141, 2012. View at Publisher · View at Google Scholar · View at Scopus
  5. J. Markovic, A. K. Anderson, and R. M. Todd, “Tuning to the significant: neural and genetic processes underlying affective enhancement of visual perception and memory,” Behavioural Brain Research, vol. 259, no. 1, pp. 229–241, 2014. View at Publisher · View at Google Scholar · View at Scopus
  6. K. Fuxe, B. Hamberger, and T. Hökfelt, “Distribution of noradrenaline nerve terminals in cortical areas of the rat,” Brain Research, vol. 8, no. 1, pp. 125–131, 1968. View at Publisher · View at Google Scholar
  7. K. C. Gatter and T. P. Powell, “The projection of the locus coeruleus upon the neocortex in the macaque monkey,” Neuroscience, vol. 2, no. 3, pp. 441–445, 1977. View at Publisher · View at Google Scholar · View at Scopus
  8. B. E. Jones and R. Y. Moore, “Ascending projections of the locus coeruleus in the rat. II. Autoradiographic study,” Brain Research, vol. 127, no. 1, pp. 25–53, 1977. View at Google Scholar
  9. R. Y. Moore and F. E. Bloom, “Central catecholamine neuron systems: anatomy and physiology of the norepinephrine and epinephrine systems,” Annual Review of Neuroscience, vol. 2, no. 1, pp. 113–168, 1979. View at Publisher · View at Google Scholar
  10. S. L. Foote, F. E. Bloom, and G. Aston-Jones, “Nucleus locus ceruleus: new evidence of anatomical and physiological specificity,” Physiological Reviews, vol. 63, no. 3, pp. 844–914, 1983. View at Google Scholar
  11. G. Aston-Jones and F. E. Bloom, “Activity of norepinephrine-containing locus coeruleus neurons in behaving rats anticipates fluctuations in the sleep-waking cycle,” Journal of Neuroscience: The Official Journal of the Society for Neuroscience, vol. 1, no. 8, pp. 876–886, 1981. View at Google Scholar
  12. D. A. McCormick, “Cholinergic and noradrenergic modulation of thalamocortical processing,” Trends in Neurosciences, vol. 12, no. 6, pp. 215–221, 1989. View at Publisher · View at Google Scholar · View at Scopus
  13. C. W. Berridge, B. E. Schmeichel, and R. A. España, “Noradrenergic modulation of wakefulness/arousal,” Sleep Medicine Reviews, vol. 16, no. 2, pp. 187–197, 2012. View at Publisher · View at Google Scholar · View at Scopus
  14. S. L. Foote, G. Aston-Jones, and F. E. Bloom, “Impulse activity of locus coeruleus neurons in awake rats and monkeys is a function of sensory stimulation and arousal,” Proceedings of the National Academy of Sciences of the United States of America, vol. 77, no. 5, pp. 3033–3037, 1980. View at Google Scholar
  15. T. W. Robbins, “Cortical noradrenaline, attention and arousal,” Psychological Medicine, vol. 14, no. 1, pp. 13–21, 1984. View at Google Scholar
  16. J. Rajkowski, P. Kubiak, and G. Aston-Jones, “Locus coeruleus activity in monkey: phasic and tonic changes are associated with altered vigilance,” Brain Research Bulletin, vol. 35, no. 5-6, pp. 607–616, 1994. View at Google Scholar
  17. C. W. Berridge, “Noradrenergic modulation of arousal,” Brain Research Reviews, vol. 58, no. 1, pp. 1–17, 2008. View at Publisher · View at Google Scholar · View at Scopus
  18. D. J. Chandler, “Evidence for a specialized role of the locus coeruleus noradrenergic system in cortical circuitries and behavioral operations,” Brain Research, vol. 1641, no. Pt B, pp. 197–206, 2016. View at Google Scholar
  19. D. A. McCormick and D. A. Prince, “Two types of muscarinic response to acetylcholine in mammalian cortical neurons,” Proceedings of the National Academy of Sciences of the United States of America, vol. 82, no. 18, pp. 6344–6348, 1985. View at Google Scholar
  20. E. Marder, “Neuromodulation of neuronal circuits: back to the future,” Neuron, vol. 76, no. 1, pp. 1–11, 2012. View at Publisher · View at Google Scholar · View at Scopus
  21. G. Aston-Jones and F. E. Bloom, “Norepinephrine-containing locus coeruleus neurons in behaving rats exhibit pronounced responses to non-noxious environmental stimuli,” Journal of Neuroscience: The Official Journal of the Society for Neuroscience, vol. 1, no. 8, pp. 887–900, 1981. View at Google Scholar
  22. G. Aston-Jones, J. Rajkowski, P. Kubiak, and T. Alexinsky, “Locus coeruleus neurons in monkey are selectively activated by attended cues in a vigilance task,” Journal of Neuroscience: The Official Journal of the Society for Neuroscience, vol. 14, no. 7, pp. 4467–4480, 1994. View at Google Scholar
  23. S. Bouret and S. J. Sara, “Locus coeruleus activation modulates firing rate and temporal organization of odour-induced single-cell responses in rat piriform cortex,” The European Journal of Neuroscience, vol. 16, no. 12, pp. 2371–2382, 2002. View at Publisher · View at Google Scholar · View at Scopus
  24. A. Vankov, A. Hervé-Minvielle, and S. J. Sara, “Response to novelty and its rapid habituation in locus coeruleus neurons of the freely exploring rat,” The European Journal of Neuroscience, vol. 7, no. 6, pp. 1180–1187, 1995. View at Publisher · View at Google Scholar · View at Scopus
  25. D. E. Redmond and Y. H. Huang, “Current concepts. II. New evidence for a locus coeruleus-norepinephrine connection with anxiety,” Life Sciences, vol. 25, no. 26, pp. 2149–2162, 1979. View at Publisher · View at Google Scholar · View at Scopus
  26. M. Tanaka, M. Yoshida, H. Emoto, and H. Ishii, “Noradrenaline systems in the hypothalamus, amygdala and locus coeruleus are involved in the provocation of anxiety: basic studies,” European Journal of Pharmacology, vol. 405, no. 1–3, pp. 397–406, 2000. View at Publisher · View at Google Scholar · View at Scopus
  27. G. Aston-Jones, J. Rajkowski, and P. Kubiak, “Conditioned responses of monkey locus coeruleus neurons anticipate acquisition of discriminative behavior in a vigilance task,” Neuroscience, vol. 80, no. 3, pp. 697–715, 1997. View at Publisher · View at Google Scholar · View at Scopus
  28. J. Rajkowski, H. Majczynski, E. Clayton, and G. Aston-Jones, “Activation of monkey locus coeruleus neurons varies with difficulty and performance in a target detection task,” Journal of Neurophysiology, vol. 92, no. 1, pp. 361–371, 2004. View at Publisher · View at Google Scholar · View at Scopus
  29. R. M. Kalwani, S. Joshi, and J. I. Gold, “Phasic activation of individual neurons in the locus ceruleus/subceruleus complex of monkeys reflects rewarded decisions to go but not stop,” Journal of Neuroscience: The Official Journal of the Society for Neuroscience, vol. 34, no. 41, pp. 13656–13669, 2014. View at Publisher · View at Google Scholar · View at Scopus
  30. K. D. Harris and A. Thiele, “Cortical state and attention,” Nature Reviews. Neuroscience, vol. 12, no. 9, pp. 509–523, 2011. View at Publisher · View at Google Scholar · View at Scopus
  31. Z. Fazlali, Y. Ranjbar-Slamloo, M. Adibi, and E. Arabzadeh, “Correlation between cortical state and locus coeruleus activity: implications for sensory coding in rat barrel cortex,” Frontiers in Neural Circuits, vol. 10, p. 14, 2016. View at Publisher · View at Google Scholar · View at Scopus
  32. G. Aston-Jones and J. D. Cohen, “An integrative theory of locus coeruleus-norepinephrine function: adaptive gain and optimal performance,” Annual Review of Neuroscience, vol. 28, no. 1, pp. 403–450, 2005. View at Publisher · View at Google Scholar · View at Scopus
  33. S. Bouret and S. J. Sara, “Network reset: a simplified overarching theory of locus coeruleus noradrenaline function,” Trends in Neurosciences, vol. 28, no. 11, pp. 574–582, 2005. View at Publisher · View at Google Scholar · View at Scopus
  34. S. Nieuwenhuis, G. Aston-Jones, and J. D. Cohen, “Decision making, the P3, and the locus coeruleus-norepinephrine system,” Psychological Bulletin, vol. 131, no. 4, pp. 510–532, 2005. View at Publisher · View at Google Scholar · View at Scopus
  35. A. F. T. Arnsten, C. D. Paspalas, N. J. Gamo, Y. Yang, and M. Wang, “Dynamic network connectivity: a new form of neuroplasticity,” Trends in Cognitive Sciences, vol. 14, no. 8, pp. 365–375, 2010. View at Publisher · View at Google Scholar · View at Scopus
  36. M. Corbetta, G. Patel, and G. L. Shulman, “The reorienting system of the human brain: from environment to theory of mind,” Neuron, vol. 58, no. 3, pp. 306–324, 2008. View at Publisher · View at Google Scholar · View at Scopus
  37. D. Servan-Schreiber, H. Printz, and J. D. Cohen, “A network model of catecholamine effects: gain, signal-to-noise ratio, and behavior,” Science, vol. 249, no. 4971, pp. 892–895, 1990. View at Publisher · View at Google Scholar
  38. M. Usher, J. D. Cohen, D. Servan-Schreiber, J. Rajkowski, and G. Aston-Jones, “The role of locus coeruleus in the regulation of cognitive performance,” Science, vol. 283, no. 5401, pp. 549–554, 1999. View at Publisher · View at Google Scholar · View at Scopus
  39. R. M. Harris-Warrick, “Neuromodulation and flexibility in central pattern generator networks,” Current Opinion in Neurobiology, vol. 21, no. 5, pp. 685–692, 2011. View at Publisher · View at Google Scholar · View at Scopus
  40. S. Bouret and S. J. Sara, “Reward expectation, orientation of attention and locus coeruleus-medial frontal cortex interplay during learning,” The European Journal of Neuroscience, vol. 20, no. 3, pp. 791–802, 2004. View at Publisher · View at Google Scholar · View at Scopus
  41. P. Dayan and A. J. Yu, “Phasic norepinephrine: a neural interrupt signal for unexpected events,” Netwrk (Bristol, England), vol. 17, no. 4, pp. 335–350, 2006. View at Google Scholar
  42. J. T. Coull, C. Büchel, K. J. Friston, and C. D. Frith, “Noradrenergically mediated plasticity in a human attentional neuronal network,” NeuroImage, vol. 10, no. 6, pp. 705–715, 1999. View at Publisher · View at Google Scholar · View at Scopus
  43. E. J. Hermans, H. J. van Marle, L. Ossewaarde et al., “Stress-related noradrenergic activity prompts large-scale neural network reconfiguration,” Science, vol. 334, no. 6059, pp. 1151–1153, 2011. View at Publisher · View at Google Scholar · View at Scopus
  44. W. W. Seeley, V. Menon, A. F. Schatzberg et al., “Dissociable intrinsic connectivity networks for salience processing and executive control,” Journal of Neuroscience: The Official Journal of the Society for Neuroscience, vol. 27, no. 9, pp. 2349–2356, 2007. View at Publisher · View at Google Scholar · View at Scopus
  45. L. Q. Uddin, “Salience processing and insular cortical function and dysfunction,” Nature Reviews. Neuroscience, vol. 16, no. 1, pp. 55–61, 2015. View at Publisher · View at Google Scholar · View at Scopus
  46. D. T. Wong, P. G. Threlkeld, K. L. Best, and F. P. Bymaster, “A new inhibitor of norepinephrine uptake devoid of affinity for receptors in rat brain,” The Journal of Pharmacology and Experimental Therapeutics, vol. 222, no. 1, pp. 61–65, 1982. View at Google Scholar
  47. F. P. Bymaster, J. S. Katner, D. L. Nelson et al., “Atomoxetine increases extracellular levels of norepinephrine and dopamine in prefrontal cortex of rat: a potential mechanism for efficacy in attention deficit/hyperactivity disorder,” Neuropsychopharmacology, vol. 27, no. 5, pp. 699–711, 2002. View at Publisher · View at Google Scholar · View at Scopus
  48. C. J. Swanson, K. W. Perry, S. Koch-Krueger, J. Katner, K. A. Svensson, and F. P. Bymaster, “Effect of the attention deficit/hyperactivity disorder drug atomoxetine on extracellular concentrations of norepinephrine and dopamine in several brain regions of the rat,” Neuropharmacology, vol. 50, no. 6, pp. 755–760, 2006. View at Publisher · View at Google Scholar · View at Scopus
  49. C. Guedj, E. Monfardini, A. J. Reynaud, A. Farnè, M. Meunier, and F. Hadj-Bouziane, “Boosting norepinephrine transmission triggers flexible reconfiguration of brain networks at rest,” Cerebral Cortex, 2016. View at Publisher · View at Google Scholar
  50. J. T. Serences and S. Yantis, “Selective visual attention and perceptual coherence,” Trends in Cognitive Sciences, vol. 10, no. 1, pp. 38–45, 2006. View at Publisher · View at Google Scholar · View at Scopus
  51. M. R. Cohen and J. H. R. Maunsell, “Attention improves performance primarily by reducing interneuronal correlations,” Nature Neuroscience, vol. 12, no. 12, pp. 1594–1600, 2009. View at Publisher · View at Google Scholar · View at Scopus
  52. J. F. Mitchell, K. A. Sundberg, and J. H. Reynolds, “Spatial attention decorrelates intrinsic activity fluctuations in macaque area V4,” Neuron, vol. 63, no. 6, pp. 879–888, 2009. View at Publisher · View at Google Scholar · View at Scopus
  53. S. L. Foote, R. Freedman, and A. P. Oliver, “Effects of putative neurotransmitters on neuronal activity in monkey auditory cortex,” Brain Research, vol. 86, no. 2, pp. 229–242, 1975. View at Publisher · View at Google Scholar · View at Scopus
  54. B. D. Waterhouse and D. J. Woodward, “Interaction of norepinephrine with cerebrocortical activity evoked by stimulation of somatosensory afferent pathways in the rat,” Experimental Neurology, vol. 67, no. 1, pp. 11–34, 1980. View at Publisher · View at Google Scholar · View at Scopus
  55. C. W. Berridge and B. D. Waterhouse, “The locus coeruleus-noradrenergic system: modulation of behavioral state and state-dependent cognitive processes,” Brain Research. Brain Research Reviews, vol. 42, no. 1, pp. 33–84, 2003. View at Publisher · View at Google Scholar · View at Scopus
  56. T. H. Donner and S. Nieuwenhuis, “Brain-wide gain modulation: the rich get richer,” Nature Neuroscience, vol. 16, no. 8, pp. 989-990, 2013. View at Publisher · View at Google Scholar · View at Scopus
  57. P. Fries, “A mechanism for cognitive dynamics: neuronal communication through neuronal coherence,” Trends in Cognitive Sciences, vol. 9, no. 10, pp. 474–480, 2005. View at Publisher · View at Google Scholar · View at Scopus
  58. B. Haider and D. A. McCormick, “Rapid neocortical dynamics: cellular and network mechanisms,” Neuron, vol. 62, no. 2, pp. 171–189, 2009. View at Publisher · View at Google Scholar · View at Scopus
  59. E. Salinas and N. M. Bentley, Eds.K. Josic, J. Rubin, M. Matias, and R. Romo, Eds., “Gain modulation as a mechanism for switching reference frames, tasks, and targets,” Coherent Behavior in Neuronal Networks, Springer, New York, 2009. View at Google Scholar
  60. M. S. Gilzenrat, B. D. Holmes, J. Rajkowski, G. Aston-Jones, and J. D. Cohen, “Simplified dynamics in a model of noradrenergic modulation of cognitive performance,” Neural Networks, vol. 15, no. 4–6, pp. 647–663, 2002. View at Google Scholar
  61. E. Shea-Brown, M. S. Gilzenrat, and J. D. Cohen, “Optimization of decision making in multilayer networks: the role of locus coeruleus,” Neural Computation, vol. 20, no. 12, pp. 2863–2894, 2008. View at Publisher · View at Google Scholar
  62. E. Eldar, J. D. Cohen, and Y. Niv, “The effects of neural gain on attention and learning,” Nature Neuroscience, vol. 16, no. 8, pp. 1146–1153, 2013. View at Publisher · View at Google Scholar · View at Scopus
  63. H. Safaai, R. Neves, O. Eschenko, N. K. Logothetis, and S. Panzeri, “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, vol. 112, no. 41, pp. 12834–12839, 2015. View at Publisher · View at Google Scholar · View at Scopus
  64. A. Zalesky, A. Fornito, I. H. Harding et al., “Whole-brain anatomical networks: does the choice of nodes matter?” NeuroImage, vol. 50, no. 3, pp. 970–983, 2010. View at Publisher · View at Google Scholar · View at Scopus
  65. S. Achard, R. Salvador, B. Whitcher, J. Suckling, and E. Bullmore, “A resilient, low-frequency, small-world human brain functional network with highly connected association cortical hubs,” The Journal of Neuroscience, vol. 26, no. 1, pp. 63–72, 2006. View at Publisher · View at Google Scholar · View at Scopus
  66. S. Achard and E. Bullmore, “Efficiency and cost of economical brain functional networks,” PLoS Computational Biology, vol. 3, no. 2, 2007. View at Publisher · View at Google Scholar · View at Scopus
  67. E. Bullmore and O. Sporns, “Complex brain networks: graph theoretical analysis of structural and functional systems,” Nature Reviews. Neuroscience, vol. 10, no. 4, pp. 312–312, 2009. View at Publisher · View at Google Scholar · View at Scopus
  68. C. M. Warren, S. Nieuwenhuis, and T. H. Donner, “Perceptual choice boosts network stability: effect of neuromodulation?” Trends in Cognitive Sciences, vol. 19, no. 7, pp. 362–364, 2015. View at Publisher · View at Google Scholar · View at Scopus
  69. R. L. van den Brink, T. Pfeffer, C. M. Warren et al., “Catecholaminergic neuromodulation shapes intrinsic MRI functional connectivity in the human brain,” The Journal of Neuroscience, vol. 36, no. 30, pp. 7865–7876, 2016. View at Publisher · View at Google Scholar · View at Scopus
  70. D. A. Leopold, Y. Murayama, and N. K. Logothetis, “Very slow activity fluctuations in monkey visual cortex: implications for functional brain imaging,” Cerebral Cortex, vol. 13, no. 4, pp. 422–433, 2003. View at Publisher · View at Google Scholar · View at Scopus
  71. P. J. Drew, J. H. Duyn, E. Golanov, and D. Kleinfeld, “Finding coherence in spontaneous oscillations,” Nature Neuroscience, vol. 11, no. 9, pp. 991–993, 2008. View at Publisher · View at Google Scholar · View at Scopus
  72. M. L. Schölvinck, A. Maier, F. Q. Ye, J. H. Duyn, and D. A. Leopold, “Neural basis of global resting-state fMRI activity,” Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 22, pp. 10238–10243, 2010. View at Publisher · View at Google Scholar · View at Scopus
  73. Y. Nir, L. Fisch, R. Mukamel et al., “Coupling between neuronal firing rate, gamma LFP, and BOLD fMRI is related to interneuronal correlations,” Current Biology: CB, vol. 17, no. 15, pp. 1275–1285, 2007. View at Publisher · View at Google Scholar · View at Scopus
  74. Y. Nir, R. Mukamel, I. Dinstein et al., “Interhemispheric correlations of slow spontaneous neuronal fluctuations revealed in human sensory cortex,” Nature Neuroscience, vol. 11, no. 9, pp. 1100–1108, 2008. View at Publisher · View at Google Scholar · View at Scopus
  75. A. Bruns, R. Eckhorn, H. Jokeit, and A. Ebner, “Amplitude envelope correlation detects coupling among incoherent brain signals,” Neuroreport, vol. 11, no. 7, pp. 1509–1514, 2000. View at Publisher · View at Google Scholar
  76. M. D. Fox and M. E. Raichle, “Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging,” Nature Reviews. Neuroscience, vol. 8, no. 9, pp. 700–711, 2007. View at Publisher · View at Google Scholar · View at Scopus
  77. B. J. He, A. Z. Snyder, J. M. Zempel, M. D. Smyth, and M. E. Raichle, “Electrophysiological correlates of the brain’s intrinsic large-scale functional architecture,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 41, pp. 16039–16044, 2008. View at Publisher · View at Google Scholar · View at Scopus
  78. A. Shmuel and D. A. Leopold, “Neuronal correlates of spontaneous fluctuations in fMRI signals in monkey visual cortex: implications for functional connectivity at rest,” Human Brain Mapping, vol. 29, no. 7, pp. 751–761, 2008. View at Publisher · View at Google Scholar · View at Scopus
  79. T. Akam and D. M. Kullmann, “Oscillatory multiplexing of population codes for selective communication in the mammalian brain,” Nature Reviews. Neuroscience, vol. 15, no. 2, pp. 111–122, 2014. View at Publisher · View at Google Scholar · View at Scopus
  80. V. S. Sohal, F. Zhang, O. Yizhar, and K. Deisseroth, “Parvalbumin neurons and gamma rhythms enhance cortical circuit performance,” Nature, vol. 459, no. 7247, pp. 698–702, 2009. View at Publisher · View at Google Scholar · View at Scopus
  81. P. Fries, D. Nikolić, and W. Singer, “The gamma cycle,” Trends in Neurosciences, vol. 30, no. 7, pp. 309–316, 2007. View at Publisher · View at Google Scholar · View at Scopus
  82. T. Womelsdorf, J. M. Schoffelen, R. Oostenveld et al., “Modulation of neuronal interactions through neuronal synchronization,” Science, vol. 316, no. 5831, pp. 1609–1612, 2007. View at Publisher · View at Google Scholar · View at Scopus
  83. T. Womelsdorf, T. A. Valiante, N. T. Sahin, K. J. Miller, and P. Tiesinga, “Dynamic circuit motifs underlying rhythmic gain control, gating and integration,” Nature Neuroscience, vol. 17, no. 8, pp. 1031–1039, 2014. View at Publisher · View at Google Scholar · View at Scopus
  84. P. Fries, “Neuronal gamma-band synchronization as a fundamental process in cortical computation,” Annual Review of Neuroscience, vol. 32, pp. 209–224, 2009. View at Publisher · View at Google Scholar · View at Scopus
  85. P. Fries, “Rhythms for cognition: communication through coherence,” Neuron, vol. 88, no. 1, pp. 220–235, 2015. View at Publisher · View at Google Scholar · View at Scopus
  86. B. Voloh and T. Womelsdorf, “A role of phase-resetting in coordinating large scale neural networks during attention and goal-directed behavior,” Frontiers in Systems Neuroscience, vol. 10, p. 18, 2016. View at Publisher · View at Google Scholar · View at Scopus
  87. B. Voloh, T. A. Valiante, S. Everling, and T. Womelsdorf, “Theta-gamma coordination between anterior cingulate and prefrontal cortex indexes correct attention shifts,” Proceedings of the National Academy of Sciences of the United States of America, vol. 112, no. 27, pp. 8457–8462, 2015. View at Publisher · View at Google Scholar · View at Scopus
  88. A. J. Yu and P. Dayan, “Uncertainty, neuromodulation, and attention,” Neuron, vol. 46, no. 4, pp. 681–692, 2005. View at Publisher · View at Google Scholar · View at Scopus
  89. L. A. Briand, H. Gritton, W. M. Howe, D. A. Young, and M. Sarter, “Modulators in concert for cognition: modulator interactions in the prefrontal cortex,” Progress in Neurobiology, vol. 83, no. 2, pp. 69–91, 2007. View at Publisher · View at Google Scholar · View at Scopus
  90. A. Bari and G. Aston-Jones, “Atomoxetine modulates spontaneous and sensory-evoked discharge of locus coeruleus noradrenergic neurons,” Neuropharmacology, vol. 64, no. 1, pp. 53–64, 2013. View at Publisher · View at Google Scholar · View at Scopus
  91. R. A. M. Brown, S. G. Walling, J. S. Milway, and C. W. Harley, “Locus ceruleus activation suppresses feedforward interneurons and reduces beta-gamma electroencephalogram frequencies while it enhances theta frequencies in rat dentate gyrus,” Journal of Neuroscience: The Official Journal of the Society for Neuroscience, vol. 25, no. 8, pp. 1985–1991, 2005. View at Publisher · View at Google Scholar · View at Scopus
  92. M. Hajós, W. E. Hoffmann, D. D. Robinson, J. H. Yu, and E. Hajós-Korcsok, “Norepinephrine but not serotonin reuptake inhibitors enhance theta and gamma activity of the septo-hippocampal system,” Neuropsychopharmacology, vol. 28, no. 5, pp. 857–864, 2003. View at Publisher · View at Google Scholar · View at Scopus
  93. V. F. Kichigina, E. S. Kutyreva, and V. V. Sudnitsyn, “Sensory responses of neurons in the medial septal area in conditions of modulation of theta activity using the alpha-2-adrenoreceptor agonist clonidine,” Neuroscience and Behavioral Physiology, vol. 35, no. 1, pp. 107–116, 2005. View at Publisher · View at Google Scholar · View at Scopus
  94. Y. Novitskaya, S. J. Sara, N. K. Logothetis, and O. Eschenko, “Ripple-triggered stimulation of the locus coeruleus during post-learning sleep disrupts ripple/spindle coupling and impairs memory consolidation,” Learning & Memory (Cold Spring Harbor, N.Y.), vol. 23, no. 5, pp. 238–248, 2016. View at Publisher · View at Google Scholar · View at Scopus
  95. A. M. Bastos, J. Vezoli, C. A. Bosman et al., “Visual areas exert feedforward and feedback influences through distinct frequency channels,” Neuron, vol. 85, no. 2, pp. 390–401, 2015. View at Publisher · View at Google Scholar · View at Scopus
  96. A. M. Bastos, J. Vezoli, and P. Fries, “Communication through coherence with inter-areal delays,” Current Opinion in Neurobiology, vol. 31, pp. 173–180, 2015. View at Publisher · View at Google Scholar · View at Scopus
  97. G. G. Gregoriou, S. J. Gotts, H. Zhou, and R. Desimone, “High-frequency, long-range coupling between prefrontal and visual cortex during attention,” Science, vol. 324, no. 5931, pp. 1207–1210, 2009. View at Publisher · View at Google Scholar · View at Scopus
  98. C. M. Gray, P. König, A. K. Engel, and W. Singer, “Oscillatory responses in cat visual cortex exhibit inter-columnar synchronization which reflects global stimulus properties,” Nature, vol. 338, no. 6213, pp. 334–337, 1989. View at Publisher · View at Google Scholar
  99. P. Fries, J. H. Reynolds, A. E. Rorie, and R. Desimone, “Modulation of oscillatory neuronal synchronization by selective visual attention,” Science, vol. 291, no. 5508, pp. 1560–1563, 2001. View at Publisher · View at Google Scholar
  100. T. Womelsdorf, P. Fries, P. P. Mitra, and R. Desimone, “Gamma-band synchronization in visual cortex predicts speed of change detection,” Nature, vol. 439, no. 7077, pp. 733–736, 2006. View at Publisher · View at Google Scholar · View at Scopus
  101. B. Pesaran, J. S. Pezaris, M. Sahani, P. P. Mitra, and R. A. Andersen, “Temporal structure in neuronal activity during working memory in macaque parietal cortex,” Nature Neuroscience, vol. 5, no. 8, pp. 805–811, 2002. View at Publisher · View at Google Scholar · View at Scopus
  102. C. S. Herrmann, M. H. J. Munk, and A. K. Engel, “Cognitive functions of gamma-band activity: memory match and utilization,” Trends in Cognitive Sciences, vol. 8, no. 8, pp. 347–355, 2004. View at Publisher · View at Google Scholar · View at Scopus
  103. M. Vinck, T. Womelsdorf, E. A. Buffalo, R. Desimone, and P. Fries, “Attentional modulation of cell-class-specific gamma-band synchronization in awake monkey area v4,” Neuron, vol. 80, no. 4, pp. 1077–1089, 2013. View at Publisher · View at Google Scholar · View at Scopus
  104. E. Başar and B. Güntekin, “A review of brain oscillations in cognitive disorders and the role of neurotransmitters,” Brain Research, vol. 1235, pp. 172–193, 2008. View at Publisher · View at Google Scholar · View at Scopus