Nuclei accumbens phase synchrony predicts decision-making reversals following negative feedback

Journal of Neuroscience

Volumn 29, Issue 23, 2009, Pages 7591-7598

  Cohen, Michael X ^a,c   Axmacher, Nikolai ^a   Lenartz, Doris ^d   Elger, Christian E ^a   Sturm, Volker ^d   Schlaepfer, Thomas E ^b,e  

^a Life and Brain Center   (Germany)

^b UNIVERSITY OF BONN   (Germany)

^c UNIVERSITY OF AMSTERDAM   (Netherlands)

^d UNIVERSITY OF COLOGNE   (Germany)

^e JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; ARTICLE; BRAIN DEPTH STIMULATION; CLINICAL ARTICLE; CONTROLLED STUDY; CORTICAL SYNCHRONIZATION; DECISION MAKING; ELECTROENCEPHALOGRAM; ELECTROPHYSIOLOGY; EVENT RELATED POTENTIAL; FEMALE; FRONTAL CORTEX; GAMMA RHYTHM; HUMAN; LEARNING; MALE; NEGATIVE FEEDBACK; NERVE POTENTIAL; NUCLEUS ACCUMBENS; OSCILLATORY POTENTIAL; PRIORITY JOURNAL; TASK PERFORMANCE; THETA RHYTHM;

ANALYSIS OF VARIANCE; CHOICE BEHAVIOR; ELECTROENCEPHALOGRAPHY; EVOKED POTENTIALS; FEMALE; FRONTAL LOBE; HUMANS; KNOWLEDGE OF RESULTS (PSYCHOLOGY); MALE; MIDDLE AGED; NERVE NET; NUCLEUS ACCUMBENS; PERIODICITY; PROBABILITY; REVERSAL LEARNING; THETA RHYTHM; TIME FACTORS;

EID: 67049142845     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5335-08.2009     Document Type: Article

References (50)

1. Block AE, Dhanji H, Thompson-Tardif SF, Floresco SB (2007) Thalamic-prefrontal cortical-ventral striatal circuitry mediates dissociable components of strategy set shifting. Cereb Cortex 17:1625-1636.
2. Brady AM, Glick SD, O'Donnell P (2005) Selective disruption of nucleus accumbens gating mechanisms in rats behaviorally sensitized to methamphetamine. J Neurosci 25:6687-6695. (Pubitemid 40995301)
3. Canolty RT, Edwards E, Dalal SS, Soltani M, Nagarajan SS, Kirsch HE, Berger MS, Barbaro NM, Knight RT (2006) High gamma power is phase-locked to theta oscillations in human neocortex. Science 313:1626-1628. (Pubitemid 44414034)
4. Chrobak JJ, Buzsáki G (1998) Gamma oscillations in the entorhinal cortex of the freely behaving rat. J Neurosci 18:388-398. (Pubitemid 28046796)
5. Cohen MX, Elger CE, Ranganath C (2007) Reward expectation modulates feedback-related negativity and EEG spectra. Neuroimage 35:968-978. (Pubitemid 46400545)
6. Cohen MX, Elger CE, Weber B (2008a) Amygdala tractography predicts functional connectivity and learning during feedback-guided decision-making. Neuroimage 39:1396-1407.
7. Cohen MX, Axmacher N, Lenartz D, Elger CE, Sturm V, Schlaepfer TE (2008b) Good vibrations: cross-frequency coupling in the human nucleus accumbens during reward processing. J Cogn Neurosci 21:875-889.
8. Cools R, Clark L, Owen AM, Robbins TW (2002) Defining the neural mechanisms of probabilistic reversal learning using event-related functional magnetic resonance imaging. J Neurosci 22:4563-4567. (Pubitemid 37465672)
9. Cools R, Altamirano L, D'Esposito M (2006) Reversal learning in Parkinson's disease depends on medication status and outcome valence. Neuropsychologia 44:1663-1673. (Pubitemid 43928015)
10. Deadwyler SA, Hayashizaki S, Cheer J, Hampson RE (2004) Reward, memory and substance abuse: functional neuronal circuits in the nucleus accumbens. Neurosci Biobehav Rev 27:703-711. (Pubitemid 38199603)
11. Epstein J, Pan H, Kocsis JH, Yang Y, Butler T, Chusid J, Hochberg H, Murrough J, Strohmayer E, Stern E, Silbersweig DA (2006) Lack of ventral striatal response to positive stimuli in depressed versus normal subjects. Am J Psychiatry 163:1784-1790. (Pubitemid 44522488)
12. Finch DM (1996) Neurophysiology of converging synaptic inputs from the rat prefrontal cortex, amygdala, midline thalamus, and hippocampal formation onto single neurons of the caudate/putamen and nucleus accumbens. Hippocampus 6:495-512. (Pubitemid 26413936)
13. Fries P (2005) A mechanism for cognitive dynamics: neuronal communication through neuronal coherence. Trends Cogn Sci 9:474-480. (Pubitemid 41338822)
14. Genovese CR, Lazar NA, Nichols T (2002) Thresholding of statistical maps in functional neuroimaging using the false discovery rate. Neuroimage 15:870-878. (Pubitemid 34852500)
15. Goto Y, Grace AA (2005) Dopaminergic modulation of limbic and cortical drive of nucleus accumbens in goal-directed behavior. Nat Neurosci 8:805-812. (Pubitemid 43085848)
16. Groenewegen HJ, Wright CI, Beijer AV (1996) The nucleus accumbens: gateway for limbic structures to reach the motor system? Prog Brain Res 107:485-511.
17. Haber SN, Kim KS, Mailly P, Calzavara R (2006) Reward-related cortical inputs define a large striatal region in primates that interface with associative cortical connections, providing a substrate for incentive-based learning. J Neurosci 26:8368-8376. (Pubitemid 44309851)
18. Jensen O, Lisman JE (1996) Hippocampal CA3 region predicts memory sequences: accounting for the phase precession of place cells. Learn Mem 3:279-287. (Pubitemid 26357752)
19. Jensen O, Lisman JE (2005) Hippocampal sequence-encoding driven by a cortical multi-item working memory buffer. Trends Neurosci 28:67-72. (Pubitemid 40178922)
20. Kasanetz F, Riquelme LA, O'Donnell P, Murer MG (2006) Turning off cortical ensembles stops striatal Up states and elicits phase perturbations in cortical and striatal slow oscillations in rat in vivo. J Physiol 577:97-113. (Pubitemid 44698243)
21. Knutson B, Adams CM, Fong GW, Hommer D (2001) Anticipation of increasing monetary reward selectively recruits nucleus accumbens. J Neurosci 21:RC159.
22. Knutson B, Bhanji JP, Cooney RE, Atlas LY, Gotlib IH (2008) Neural responses to monetary incentives in major depression. Biol Psychiatry 63:686-692. (Pubitemid 351329276)
23. Lachaux JP, Rodriguez E, Martinerie J, Varela FJ (1999) Measuring phase synchrony in brain signals. Hum Brain Mapp 8:194-208.
24. Lakatos P, Shah AS, Knuth KH, Ulbert I, Karmos G, Schroeder CE (2005) An oscillatory hierarchy controlling neuronal excitability and stimulus processing in the auditory cortex. J Neurophysiol 94:1904-1911. (Pubitemid 41192862)
25. Lisman JE (2005) The theta/gamma discrete phase code occuring during the hippocampal phase precession may be a more general brain coding scheme. Hippocampus 15:913-922. (Pubitemid 41556421)
26. Marco-Pallares J, Cucurell D, Cunillera T, García R, Andrés-Pueyo A, Münte TF, Rodríguez-Fornells A (2008) Human oscillatory activity associated to reward processing in a gambling task. Neuropsychologia 46:241-248.
27. Mayberg HS, Lozano AM, Voon V, McNeely HE, Seminowicz D, Hamani C, Schwalb JM, Kennedy SH (2005) Deep brain stimulation for treatment-resistant depression. Neuron 45:651-660. (Pubitemid 40320700)
28. McClure SM, Berns GS, Montague PR (2003) Temporal prediction errors in a passive learning task activate human striatum. Neuron 38:339-346. (Pubitemid 36555658)
29. McCracken CB, Grace AA (2007) High-frequency deep brain stimulation of the nucleus accumbens region suppresses neuronal activity and selectively modulates afferent drive in rat orbitofrontal cortex in vivo. J Neurosci 27:12601-12610. (Pubitemid 350127827)
30. McIntyre CC, Savasta M, Kerkerian-Le Goff L, Vitek JL (2004) Uncovering the mechanism(s) of action of deep brain stimulation: activation, inhibition, or both. Clin Neurophysiol 115:1239-1248. (Pubitemid 38596707)
31. Mogenson GJ, Jones DL, Yim CY (1980) From motivation to action: functional interface between the limbic system and the motor system. Prog Neurobiol 14:69-97. (Pubitemid 10053405)
32. Mogenson GJ, Swanson LW, Wu M (1983) Neural projections from nucleus accumbens to globus pallidus, substantia innominata, and lateral preoptic-lateral hypothalamic area: an anatomical and electrophysiological investigation in the rat. J Neurosci 3:189-202. (Pubitemid 13193402)
33. Mormann F, Fell J, Axmacher N, Weber B, Lehnertz K, Elger CE, Fernández G (2005) Phase/amplitude reset and theta-gamma interaction in the human medial temporal lobe during a continuous word recognition memory task. Hippocampus 15:890-900. (Pubitemid 41556419)
34. Münte TF, Heldman M, Hinrichs H, Marco-Pallares J, Kraemer UM, Sturm V, Heinze HJ (2008) Nucleus accumbens is involved in human action monitoring: evidence from invasive electrophysiological recordings. Front Hum Neurosci 1:2-14.
35. O'Donnell P, Grace AA (1995) Synaptic interactions among excitatory afferents to nucleus accumbens neurons: hippocampal gating of prefrontal cortical input. J Neurosci 15:3622-3639.
36. Paz R, Pelletier JG, Bauer EP, Paré D (2006) Emotional enhancement of memory via amygdala-driven facilitation of rhinal interactions. Nat Neurosci 9:1321-1329. (Pubitemid 44454274)
37. Pesaran B, Nelson MJ, Andersen RA (2008) Free choice activates a decision circuit between frontal and parietal cortex. Nature 453:406-409. (Pubitemid 351693121)
38. Plenz D, Kitai ST (1998) Up and down states in striatal medium spiny neurons simultaneously recorded with spontaneous activity in fast-spiking interneurons studied in cortex-striatum-substantia nigra organotypic cultures. J Neurosci 18:266-283. (Pubitemid 28046787)
39. Pothuizen HH, Jongen-Rêlo AL, Feldon J, Yee BK (2005) Double dissociation of the effects of selective nucleus accumbens core and shell lesions on impulsive-choice behaviour and salience learning in rats. Eur J Neurosci 22:2605-2616. (Pubitemid 41759003)
40. Schlaepfer TE, Cohen MX, Frick C, Kosel M, Brodesser D, Axmacher N, Joe AY, Kreft M, Lenartz D, Sturm V (2008) Deep brain stimulation to reward circuitry alleviates anhedonia in refractory major depression. Neuropsychopharmacology 33:368-377. (Pubitemid 350243349)
41. Schoenbaum G, Setlow B (2003) Lesions of nucleus accumbens disrupt learning about aversive outcomes. J Neurosci 23:9833-9841. (Pubitemid 37371597)
42. Steriade M (2006) Grouping of brain rhythms in corticothalamic systems. Neuroscience 137:1087-1106. (Pubitemid 43133136)
43. Sturm V, Lenartz D, Koulousakis A, Treuer H, Herholz K, Klein JC, Klosterkötter J (2003) The nucleus accumbens: a target for deep brain stimulation in obsessive-compulsive- and anxiety-disorders. J Chem Neuroanat 26:293-299. (Pubitemid 38077152)
44. Tabuchi ET, Mulder AB, Wiener SI (2000) Position and behavioral modulation of synchronization of hippocampal and accumbens neuronal discharges in freely moving rats. Hippocampus 10:717-728. (Pubitemid 32045825)
45. Tort AB, Rotstein HG, Dugladze T, Gloveli T, Kopell NJ (2007) On the formation of gamma-coherent cell assemblies by oriens lacunosum-moleculare interneurons in the hippocampus. Proc Natl Acad Sci U S A 104:13490-13495. (Pubitemid 47293972)
46. Tort AB, Kramer MA, Thorn C, Gibson DJ, Kubota Y, Graybiel AM, Kopell NJ (2008) Dynamic cross-frequency couplings of local field potential oscillations in rat striatum and hippocampus during performance of a T-maze task. Proc Natl Acad Sci U S A 105:20517-20522.
47. Varela F, Lachaux JP, Rodriguez E, Martinerie J (2001) The brainweb: phase synchronization and large-scale integration. Nat Rev Neurosci 2:229-239. (Pubitemid 33673064)
48. Winer BJ (1971) Statistical principles in experimental design: design and analysis of factorial experiments. New York: McGraw-Hill.
49. Yacubian J, Gläscher J, Schroeder K, Sommer T, Braus DF, Büchel C (2006) Dissociable systems for gain- and loss-related value predictions and errors of prediction in the human brain. J Neurosci 26:9530-9537. (Pubitemid 44396866)
50. Yavich L, MacDonald E (2000) Dopamine release from pharmacologically distinct storage pools in rat striatum following stimulation at frequency of neuronal bursting. Brain Res 870:73-79. (Pubitemid 30408405)