Desynchronization and rebound of beta oscillations during conscious and unconscious local neuronal processing in the macaque lateral prefrontal cortex

Frontiers in Psychology

Volumn 4, Issue SEP, 2013, Pages

  Panagiotaropoulos, Theofanis I ^a   Kapoor, Vishal ^a   Logothetis, Nikos K ^a,b  

^a MAX PLANCK INSTITUTE FOR BIOLOGICAL CYBERNETICS   (Germany)

^b UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

Beta oscillations; Consciousness; Control; Prefrontal cortex

Indexed keywords

EID: 84885344682     PISSN: None     EISSN: 16641078     Source Type: Journal    
DOI: 10.3389/fpsyg.2013.00603     Document Type: Article

References (62)

1. Baker, S. N., Kilner, J. M., Pinches, E. M., and Lemon, R. N. (1999). The role of synchrony and oscillations in the motor output. Exp. Brain Res. 128, 109-117. doi:10.1007/s002210050825.
2. Baker, S. N. (2007). Oscillatory interactions between sensorimotor cortex and the periphery. Curr. Opin. Neurobiol. 17, 649-655. doi:10.1016/j.conb.2008.01.007.
3. Berens, P., Keliris, G. A., Ecker, A. S., Logothetis, N. K., and Tolias, A. S. (2008). Comparing the feature selectivity of the gamma-band of the local field potential and the underlying spiking activity in primate visual cortex. Front. Syst. Neurosci. 2:2. doi:10.3389/neuro.06.002.2008.
4. Belitski, A., Gretton, A., Magri, A., Murayama, Y., Montemurro, M. A., Logothetis, N. K., et al. (2008). Low-frequency local field potentials and spikes in primary visual cortex convey independent visual information. J. Neurosci. 28, 5696-5709. doi:10.1523/JNEUROSCI.0009-08.2008.
5. Berns, G. S., Cohen, J. D., and Mintun, M. A. (1997). Brain regions responsive to novelty in the absence of awareness. Science 276, 1272-1275. doi:10.1126/science.276.5316.1272.
6. Brown, P. (2007). Abnormal oscillatory synchronization in the motor system leads to impaired movement. Curr. Opin. Neurobiol. 17, 656-664. doi:10.1016/j.conb.2007.12.001.
7. Buschman, T. J., and Miller, E. K. (2007). Top-down versus bottom-up control of attention in the prefrontal and posterior parietal cortices. Science 315, 1860-1862. doi:10.1126/science.1138071.
8. Buschman, T. J., and Miller, E. K. (2009). Serial, covert shifts of attention during visual search are reflected by the frontal eye fields and correlated with population oscillations. Neuron 63, 386-396. doi:10.1016/j.neuron.2009.06.020.
9. Buschman, T. J., Denovellis, E. L., Diogo, C., Bullock, D., and Miller, E. K. (2012). Synchronous oscillatory neural ensembles for rules in the prefrontal cortex. Neuron 76, 838-846. doi:10.1016/j.neuron.2012.09.029.
10. Chen, C. C., Litvak, V., Gilbertson, T., Kühn, A., Lu, C. S., Lee, S. T., et al. (2007). Excessive synchronization of basal ganglia neurons at 20 Hz slows movement in Parkinson's disease. Exp. Neurol. 205, 214-221. doi:10.1016/j.expneurol.2007.01.027.
11. Dehaene, S., and Changeux, J. P. (2011). Experimental and theoretical approaches to conscious processing. Neuron 70, 200-227. doi:10.1016/j.neuron.2011.03.018.
12. Donoghue, J. P., Sanes, J. N., Hatsopoulos, N. G., and Gaál, G. (1998). Neural discharge and local field potential oscillations in primate motor cortex during voluntary movements. J. Neurophysiol. 79, 159-173.
13. Eimer, M. (1999). Facilitatory and inhibitory effects of masked prime stimuli on motor activation and behavioural performance. Acta Psychol. (Amst.) 101, 293-313. doi:10.1016/S0001-6918(99)00009-8.
14. Eimer, M., and Schlaghecken, F. (1998). Effects of masked stimuli on motor activation:behavioral and electrophysiological evidence. J. Exp. Psychol. Hum. Percept. Perform. 24, 1737-1747. doi:10.1037/0096-1523.24.6.1737.
15. Engel, A. K., and Fries, P. (2010). Beta-band oscillations-signalling the status quo? Curr. Opin. Neurobiol. 20, 156-165. doi:10.1016/j.conb.2010.02.015.
16. Frien, A., Eckhorn, R., Bauer, R., Woelbern, T., and Gabriel, A. (2000). Fast oscillations display sharper orientation tuning than slower components of the same recordings in striate cortex of the awake monkey. Eur. J. Neurosci. 12, 1453-1465. doi:10.1046/j.1460-9568.2000.00025.x.
17. Gail, A., Brinksmeyer, H. J., and Eckhorn, R. (2004). Perception-related modulations of local field potential power and coherence in primary visual cortex of awake monkey during binocular rivalry. Cereb. Cortex 14, 300-313. doi:10.1093/cercor/bhg129.
18. Gaillard, R., Dehaene, S., Adam, C., Clémenceau, S., Hasboun, D., Baulac, M., et al. (2009). Converging intracranial markers of conscious access. PLoS Biol. 7:e1000061. doi:10.1371/journal.pbio.1000061.
19. Gilbertson, T., Lalo, E., Doyle, L., Di Lazzaro, V., Cioni, B., and Brown, P. (2005). Existing motor state is favored at the expense of new movement during 13-35 Hz oscillatory synchrony in the human corticospinal system. J. Neurosci. 25, 7771-7779. doi:10.1523/JNEUROSCI.1762-05.2005.
20. Goldman-Rakic, P. S., Bates, J. F., and Chafee, M. V. (1992). The prefrontal cortex and internally generated motor acts. Curr. Opin. Neurobiol. 2, 830-835. doi:10.1016/0959-4388(92)90141-7.
21. Hammond, C., Bergman, H., and Brown, P. (2007). Pathological synchronization in Parkinson's disease:networks, models and treatments. Trends Neurosci. 30, 357-364. doi:10.1016/j.tins.2007.05.004.
22. Henrie, J. A., and Shapley, R. (2005). LFP power spectra in V1 cortex:the graded effect of stimulus contrast. J. Neurophysiol. 94, 479-490. doi:10.1152/jn.00919.2004.
23. Hommel, B. (2007). Consciousness and control. Not identical twins. J. Conscious. Stud. 14, 155-176.
24. Hommel, B. (2013). Dancing in the dark:no role for consciousness in action control. Front. Psychol. 4:380. doi:10.3389/fpsyg.2013.00380.
25. Jurkiewicz, M. T., Gaetz, W. C., Bostan, A. C., and Cheyne, D. (2006). Post-movement beta rebound is generated in motor cortex:evidence from neuromagnetic recordings. Neuroimage 32, 1281-1289. doi:10.1016/j.neuroimage.2006.06.005.
26. Keliris, G. A., Logothetis, N. K., and Tolias, A. S. (2010). The role of the primary visual cortex in perceptual suppression of salient visual stimuli. J. Neurosci. 30, 12353-12365. doi:10.1523/JNEUROSCI.0677-10.2010.
27. Kilavik, B. E., Zaepffel, M., Brovelli, A., Mackay, W. A., and Riehle, A. (2013). The ups and downs of beta oscillations in sensorimotor cortex. Exp. Neurol. 245, 15-26. doi:10.1016/j.expneurol.2012.09.014.
28. Kreiman, G., Fried, I., and Koch, C. (2002). Single-neuron correlates of subjective vision in the human medial temporal lobe. Proc. Natl. Acad. Sci. U.S.A. 99, 8378-8383. doi:10.1073/pnas.072194099.
29. Lau, H. C., and Passingham, R. E. (2007). Unconscious activation of the cognitive control system in the human prefrontal cortex. J. Neurosci. 27, 5805-5811. doi:10.1523/JNEUROSCI.4335-06.2007.
30. Leopold, D. A., and Logothetis, N. K. (1996). Activity changes in early visual cortex reflect monkeys' percepts during binocular rivalry. Nature 379, 549-553. doi:10.1038/379549a0.
31. Libedinsky, C., and Livingstone, M. (2011). Role of prefrontal cortex in conscious visual perception. J. Neurosci. 31, 64-69. doi:10.1523/JNEUROSCI.3620-10.2011.
32. Liu, J., and Newsome, W. T. (2006). Local field potential in cortical area MT:stimulus tuning and behavioral correlations. J. Neurosci. 26, 7779-7790. doi:10.1523/JNEUROSCI.5052-05.2006.
33. Logothetis, N. K., and Schall, J. D. (1989). Neuronal correlates of subjective visual perception. Science 245, 761-763. doi:10.1126/science.2772635.
34. Lumer, E. D., Friston, K. J., and Rees, G. (1998). Neural correlates of perceptual rivalry in the human brain. Science 280, 1930-1934. doi:10.1126/science.280.5371.1930.
35. Luria, A. R. (1969). "Frontal lobe syndromes," in Handbook of Clinical Neurology, Vol. 2, eds P. J. Vinken and G. W. Bruyn (New York, NY:Elsevier), 725-757.
36. Magri, C., Schridde, U., Murayama, Y., Panzeri, S., and Logothetis, N. K. (2012). The amplitude and timing of the BOLD signal reflects the relationship between local field potential power at different frequencies. J. Neurosci. 32, 1395-1407. doi:10.1523/JNEUROSCI.3985-11.2012.
37. Marsden, J. F., Limousin-Dowsey, J. F., Ashby, P., Pollak, P., and Brown, P. (2001). Subthalamic nucleus, sensorimotor cortex and muscle interrelationships in Parkinson's disease. Brain 124, 378-388. doi:10.1093/brain/124.2.378.
38. Mayr, U. (2004). Conflict, consciousness, and control. Trends Cogn. Sci. 8, 145-148. doi:10.1016/j.tics.2004.02.006.
39. Miller, E. K. (1999). The prefrontal cortex:complex neural properties for complex behavior. Neuron 22, 15-17. doi:10.1016/S0896-6273(00)80673-X.
40. Miller, E. K., and Cohen, J. D. (2001). An integrative theory of prefrontal cortex function. Annu. Rev. Neurosci. 24, 167-202. doi:10.1146/annurev.neuro.24.1.167.
41. Miller, E. K. (2000). The prefrontal cortex and cognitive control. Nat. Rev. Neurosci. 1, 59-65. doi:10.1038/35036228.
42. Norman, D. A., and Shallice, T. (1986). "Attention to action:willed and automatic control of behavior," in Consciousness and Self-Regulation, Vol. 4, eds R. J. Davidson, G. E. Schwartz and D. Shapiro (New York, NY:Plenum Press), 1-14.
43. O'Leary, J. G., and Hatsopoulos, N. G. (2006). Early visuomotor representations revealed from evoked local field potentials in motor and premotor cortical areas. J. Neurophysiol. 96, 1492-1506. doi:10.1152/jn.00106.2006.
44. Panagiotaropoulos, T. I., Deco, G., Kapoor, V., and Logothetis, N. K. (2012). Neuronal discharges and gamma oscillations explicitly reflect visual consciousness in the lateral prefrontal cortex. Neuron 74, 924-935. doi:10.1016/j.neuron.2012.04.013.
45. Pfurtscheller, G., Stancák, A., and Jr, Neuper, C. (1996). Post-movement beta synchronization. A correlate of an idling motor area? Electroencephalogr. Clin. Neurophysiol. 98, 281-293. doi:10.1016/0013-4694(95)00258-8.
46. Pogosyan, A., Gaynor, L. D., Eusebio, A., and Brown, P. (2009). Boosting cortical activity at beta-band frequencies slows movement in humans Curr. Biol. 19, 1637-1641. doi:10.1016/j.cub.2009.07.074.
47. Puig, M. V., and Miller, E. K. (2012). The role of prefrontal dopamine D1 receptors in the neural mechanisms of associative learning. Neuron 74, 874-886. doi:10.1016/j.neuron.2012.04.018.
48. Sanes, J. N., and Donoghue, J. P. (1993). Oscillations in local field potentials of the primate motor cortex during voluntary movement. Proc. Natl. Acad. Sci. U.S.A. 90, 4470-4474. doi:10.1073/pnas.90.10.4470.
49. Sheinberg, D. L., and Logothetis, N. K. (1997). The role of temporal cortical areas in perceptual organization. Proc. Natl. Acad. Sci. U.S.A. 94, 3408-3413. doi:10.1073/pnas.94.7.3408.
50. Siegel, M., Warden, M. R., and Miller, E. K. (2009). Phase-dependent neuronal coding of objects in short-term memory. Proc. Natl. Acad. Sci. U.S.A. 106, 21341-21346. doi:10.1073/pnas.0908193106.
51. Stephan, K. M., Thaut, M. H., Wunderlich, G., Schicks, W., Tian, B., Tellmann, L., et al. (2002). Conscious and subconscious sensorimotor synchronization-prefrontal cortex and the influence of awareness. Neuroimage 15, 345-352. doi:10.1006/nimg.2001.0929.
52. Sterzer, P., and Kleinschmidt, A. (2007). A neural basis for inference in perceptual ambiguity. Proc. Natl. Acad. Sci. U.S.A. 104, 323-328. doi:10.1073/pnas.0609006104.
53. Swann, N., Tandon, N., Canolty, R., Ellmore, T. M., McEvoy, L. K., Dreyer, S., et al. (2009). Intracranial EEG reveals a time-and frequency-specific role for the right inferior frontal gyrus and primary motor cortex in stopping initiated responses. J. Neurosci. 29, 12675-12685. doi:10.1523/JNEUROSCI.3359-09.2009.
54. Tanji, J., and Hoshi, E. (2008). Role of the lateral prefrontal cortex in executive behavioral control. Physiol. Rev. 88, 37-57. doi:10.1152/physrev.00014.2007.
55. Thomson, D. J. (1982). Spectrum estimation and harmonic-analysis. Proc. IEEE 70, 1055-1096. doi:10.1109/PROC.1982.12433.
56. van Gaal, S., de Lange, F. P., and Cohen, M. X. (2012). The role of consciousness in cognitive control and decision making. Front. Hum. Neurosci. 6:121. doi:10.3389/fnhum.2012.00121.
57. van Gaal, S., Ridderinkhof, K. R., Fahrenfort, J. J., Scholte, H. S., and Lamme, V. A. (2008). Frontal cortex mediates unconsciously triggered inhibitory control. J. Neurosci. 28, 8053-8062. doi:10.1523/JNEUROSCI.1278-08.2008.
58. van Gaal, S., Ridderinkhof, K. R., Scholte, H. S., and Lamme, V. A. (2010). Unconscious activation of the prefrontal no-go network. J. Neurosci. 30, 4143-4150. doi:10.1523/JNEUROSCI.2992-09.2010.
59. van Gaal, and S., Lamme, V. A. (2012). Unconscious high-level information processing:implication for neurobiological theories of consciousness. Neuroscientist 18, 287-301. doi:10.1177/1073858411404079.
60. Wallis, J. D., Anderson, K. C., and Miller, E. K.,(2001). Single neurons in prefrontal cortex encode abstract rules. Nature 411, 953-956. doi:10.1038/35082081.
61. White, I. M., and Wise, S. P. (1999). Rule-dependent neuronal activity in the prefrontal cortex. Exp. Brain Res. 126, 315-335. doi:10.1007/s002210050740.
62. Wolfe, J. M. (1984). Reversing ocular dominance and suppression in a single flash. Vision Res. 24, 471-478. doi:10.1016/0042-6989(84)90044-0.