Ventromedial prefrontal cortex drives hippocampal theta oscillations induced by mismatch computations

NeuroImage

Volumn 120, Issue , 2015, Pages 362-370

  Garrido, Marta I ^a   Barnes, Gareth R ^b   Kumaran, Dharshan ^c   Maguire, Eleanor A ^b   Dolan, Raymond J ^b  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Connectivity; Hippocampus; MEG; Mismatch; Novelty; Prediction; Theta entrainment; Uncertainty; Ventromedial prefrontal cortex

Indexed keywords

ADULT; ARTICLE; CONNECTOME; EVOKED VISUAL RESPONSE; FEMALE; HIPPOCAMPUS THETA RHYTHM; HUMAN; HUMAN EXPERIMENT; MAGNETOENCEPHALOGRAPHY; MALE; MISMATCH COMPUTATION; NEUROMODULATION; NORMAL HUMAN; OSCILLATION; PRIORITY JOURNAL; SIGNAL DETECTION; TASK PERFORMANCE; VENTROMEDIAL PREFRONTAL CORTEX; VISUAL STIMULATION; HIPPOCAMPUS; MIDDLE AGED; PHYSIOLOGY; PREFRONTAL CORTEX; PROCEDURES; PSYCHOMOTOR PERFORMANCE; THETA RHYTHM; YOUNG ADULT;

ADULT; FEMALE; HIPPOCAMPUS; HUMANS; MAGNETOENCEPHALOGRAPHY; MALE; MIDDLE AGED; PREFRONTAL CORTEX; PSYCHOMOTOR PERFORMANCE; THETA RHYTHM; YOUNG ADULT;

EID: 84938693182     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2015.07.016     Document Type: Article

References (67)

1. Anderson K.L., Rajagovindan R., Ghacibeh G.A., Meador K.J., Ding M. Theta oscillations mediate interaction between prefrontal cortex and medial temporal lobe in human memory. Cereb. Cortex 2010, 20:1604-1612.
2. Attal Y., Schwartz D. Assessment of subcortical source localization using deep brain activity imaging model with minimum norm operators: a MEG study. PLoS One 2013, 8. e59856.
3. Attal Y., Bhattacharjee M., Yelnik J., Cottereau B., Lefevre J., Okada Y., Bardinet E., Chupin M., Baillet S. Modeling and detecting deep brain activity with MEG & EEG. Conf Proc IEEE Eng Med Biol Soc 2007 2007, 4937-4940.
4. Axmacher N., Cohen M.X., Fell J., Haupt S., Dumpelmann M., Elger C.E., Schlaepfer T.E., Lenartz D., Sturm V., Ranganath C. Intracranial EEG correlates of expectancy and memory formation in the human hippocampus and nucleus accumbens. Neuron 2010, 65:541-549.
5. Barnes G.R., Hillebrand A., Fawcett I.P., Singh K.D. Realistic spatial sampling for MEG beamformer images. Hum. Brain Mapp. 2004, 23:120-127.
6. Boelen P.A., Reijntjes A. Intolerance of uncertainty and social anxiety. J. Anxiety Disord. 2009, 23:130-135.
7. Bonnici H.M., Chadwick M.J., Lutti A., Hassabis D., Weiskopf N., Maguire E.A. Detecting representations of recent and remote autobiographical memories in vmPFC and hippocampus. J. Neurosci. 2012, 32:16982-16991.
8. Brincat S.L., Miller E.K. Frequency-specific hippocampal-prefrontal interactions during associative learning. Nat. Neurosci. 2015, 18:576-581.
9. Brockmann M.D., Poschel B., Cichon N., Hanganu-Opatz I.L. Coupled oscillations mediate directed interactions between prefrontal cortex and hippocampus of the neonatal rat. Neuron 2011, 71:332-347.
10. Broome M.R., Johns L.C., Valli I., Woolley J.B., Tabraham P., Brett C., Valmaggia L., Peters E., Garety P.A., McGuire P.K. Delusion formation and reasoning biases in those at clinical high risk for psychosis. Br. J. Psychiatry Suppl. 2007, 51:s38-s42.
11. Brown M.W., Aggleton J.P. Recognition memory: what are the roles of the perirhinal cortex and hippocampus?. Nat. Rev. Neurosci. 2001, 2:51-61.
12. Cavada C., Company T., Tejedor J., Cruz-Rizzolo R.J., Reinoso-Suarez F. The anatomical connections of the macaque monkey orbitofrontal cortex. A review. Cereb Cortex 2000, 10:220-242.
13. Chen C.C., Kiebel S.J., Friston K.J. Dynamic causal modelling of induced responses. NeuroImage 2008, 41:1293-1312.
14. Chen J., Dastjerdi M., Foster B.L., LaRocque K.F., Rauschecker A.M., Parvizi J., Wagner A.D. Human hippocampal increases in low-frequency power during associative prediction violations. Neuropsychologia 2013, 51:2344-2351.
15. Cornwell B.R., Johnson L.L., Holroyd T., Carver F.W., Grillon C. Human hippocampal and parahippocampal theta during goal-directed spatial navigation predicts performance on a virtual Morris water maze. J. Neurosci. 2008, 28:5983-5990.
16. Cornwell B.R., Arkin N., Overstreet C., Carver F.W., Grillon C. Distinct contributions of human hippocampal theta to spatial cognition and anxiety. Hippocampus 2012, 22:1848-1859.
17. David O., Kiebel S.J., Harrison L.M., Mattout J., Kilner J.M., Friston K.J. Dynamic causal modeling of evoked responses in EEG and MEG. NeuroImage 2006, 30:1255-1272.
18. Doeller C.F., King J.A., Burgess N. Parallel striatal and hippocampal systems for landmarks and boundaries in spatial memory. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:5915-5920.
19. Duzel E., Penny W.D., Burgess N. Brain oscillations and memory. Curr. Opin. Neurobiol. 2010, 20:143-149.
20. Eickhoff S.B., Stephan K.E., Mohlberg H., Grefkes C., Fink G.R., Amunts K., Zilles K. A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data. NeuroImage 2005, 25:1325-1335.
21. Fox M.D., Snyder A.Z., Vincent J.L., Corbetta M., Van Essen D.C., Raichle M.E. The human brain is intrinsically organized into dynamic, anticorrelated functional networks. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:9673-9678.
22. Friston K. A theory of cortical responses. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2005, 360:815-836.
23. Friston K.J., Harrison L., Penny W. Dynamic causal modelling. NeuroImage 2003, 19:1273-1302.
24. Garrido M.I., Kilner J.M., Stephan K.E., Friston K.J. The mismatch negativity: a review of underlying mechanisms. Clin. Neurophysiol. 2009, 120:453-463.
25. Garrido M.I., Sahani M., Dolan R.J. Outlier responses reflect sensitivity to statistical structure in the human brain. PLoS Comput. Biol. 2013, 9. e1002999.
26. Gross J., Timmermann L., Kujala J., Salmelin R., Schnitzler A. Properties of MEG tomographic maps obtained with spatial filtering. NeuroImage 2003, 19:1329-1336.
27. Guitart-Masip M., Barnes G.R., Horner A., Bauer M., Dolan R.J., Duzel E. Synchronization of medial temporal lobe and prefrontal rhythms in human decision making. J. Neurosci. 2013, 33:442-451.
28. Hassabis D., Kumaran D., Maguire E.A. Using imagination to understand the neural basis of episodic memory. J. Neurosci. 2007, 27:14365-14374.
29. Hasselmo M.E., Stern C.E. Theta rhythm and the encoding and retrieval of space and time. NeuroImage 2014, 85(Pt 2):656-666.
30. Hillebrand A., Barnes G.R. A quantitative assessment of the sensitivity of whole-head MEG to activity in the adult human cortex. NeuroImage 2002, 16:638-650.
31. Hsieh L.T., Ranganath C. Frontal midline theta oscillations during working memory maintenance and episodic encoding and retrieval. NeuroImage 2014, 85(Pt 2):721-729.
32. Hyman J.M., Hasselmo M.E., Seamans J.K. What is the functional relevance of prefrontal cortex entrainment to hippocampal theta rhythms?. Front. Neurosci. 2011, 5:24.
33. Jeewajee A., Lever C., Burton S., O'Keefe J., Burgess N. Environmental novelty is signaled by reduction of the hippocampal theta frequency. Hippocampus 2008, 18:340-348.
34. Kersten D., Mamassian P., Yuille A. Object perception as Bayesian inference. Annu. Rev. Psychol. 2004, 55:271-304.
35. Kohler S., Danckert S., Gati J.S., Menon R.S. Novelty responses to relational and non-relational information in the hippocampus and the parahippocampal region: a comparison based on event-related fMRI. Hippocampus 2005, 15:763-774.
36. Kumaran D., Maguire E.A. An unexpected sequence of events: mismatch detection in the human hippocampus. PLoS Biol. 2006, 4. e424.
37. Kumaran D., Maguire E.A. Which computational mechanisms operate in the hippocampus during novelty detection?. Hippocampus 2007, 17:735-748.
38. Kumaran D., Maguire E.A. Novelty signals: a window into hippocampal information processing. Trends Cogn. Sci. 2009, 13:47-54.
39. Lesting J., Daldrup T., Narayanan V., Himpe C., Seidenbecher T., Pape H.C. Directional theta coherence in prefrontal cortical to amygdalo-hippocampal pathways signals fear extinction. PLoS One 2013, 8. e77707.
40. Lisman J.E., Grace A.A. The hippocampal-VTA loop: controlling the entry of information into long-term memory. Neuron 2005, 46:703-713.
41. Litvak V., Mattout J., Kiebel S., Phillips C., Henson R., Kilner J., Barnes G., Oostenveld R., Daunizeau J., Flandin G., Penny W., Friston K. EEG and MEG data analysis in SPM8. Comput. Intell. Neurosci. 2011, 2011:852961.
42. Mackey S., Petrides M. Quantitative demonstration of comparable architectonic areas within the ventromedial and lateral orbital frontal cortex in the human and the macaque monkey brains. Eur. J. Neurosci. 2010, 32:1940-1950.
43. Maguire E.A. Memory consolidation in humans: new evidence and opportunities. Exp. Physiol. 2014, 99:471-486.
44. Moran R.J., Stephan K.E., Seidenbecher T., Pape H.C., Dolan R.J., Friston K.J. Dynamic causal models of steady-state responses. NeuroImage 2009, 44:796-811.
45. Murty V.P., Adcock R.A. Enriched encoding: reward motivation organizes cortical networks for hippocampal detection of unexpected events 2013, Cereb Cortex.
46. Nieuwenhuis I.L., Takashima A. The role of the ventromedial prefrontal cortex in memory consolidation. Behav. Brain Res. 2011, 218:325-334.
47. Nolte G. The magnetic lead field theorem in the quasi-static approximation and its use for magnetoencephalography forward calculation in realistic volume conductors. Phys. Med. Biol. 2003, 48:3637-3652.
48. Penny W.D., Litvak V., Fuentemilla L., Duzel E., Friston K. Dynamic causal models for phase coupling. J. Neurosci. Methods 2009, 183:19-30.
49. Poch C., Fuentemilla L., Barnes G.R., Duzel E. Hippocampal theta-phase modulation of replay correlates with configural-relational short-term memory performance. J. Neurosci. 2011, 31:7038-7042.
50. Poppenk J., Evensmoen H.R., Moscovitch M., Nadel L. Long-axis specialization of the human hippocampus. Trends Cogn. Sci. 2013, 17:230-240.
51. Quiroga R.Q. Concept cells: the building blocks of declarative memory functions. Nat. Rev. Neurosci. 2012, 13:587-597.
52. Quraan M.A., Moses S.N., Hung Y., Mills T., Taylor M.J. Detection and localization of hippocampal activity using beamformers with MEG: a detailed investigation using simulations and empirical data. Hum. Brain Mapp. 2011, 32:812-827.
53. Ranganath C., Rainer G. Neural mechanisms for detecting and remembering novel events. Nat. Rev. Neurosci. 2003, 4:193-202.
54. Rao R.P., Ballard D.H. Predictive coding in the visual cortex: a functional interpretation of some extra-classical receptive-field effects. Nat. Neurosci. 1999, 2:79-87.
55. Roy M., Shohamy D., Wager T.D. Ventromedial prefrontal-subcortical systems and the generation of affective meaning. Trends Cogn. Sci. 2012, 16:147-156.
56. Sekihara K., Nagarajan S.S., Poeppel D., Marantz A. Asymptotic SNR of scalar and vector minimum-variance beamformers for neuromagnetic source reconstruction. IEEE Trans. Biomed. Eng. 2004, 51:1726-1734.
57. Siapas A.G., Lubenov E.V., Wilson M.A. Prefrontal phase locking to hippocampal theta oscillations. Neuron 2005, 46:141-151.
58. Singh K.D., Holliday I.E., Furlong P.L., Harding G.F.A. Evaluation of MRI-MEG/EEG co-registration strategies using Monte Carlo simulation. Electroencephalogr. Clin. Neurophysiol. 1997, 102:81-85.
59. Stephan K.E., Penny W.D., Daunizeau J., Moran R.J., Friston K.J. Bayesian model selection for group studies. NeuroImage 2009, 46:1004-1017.
60. Strange B.A., Dolan R.J. Adaptive anterior hippocampal responses to oddball stimuli. Hippocampus 2001, 11:690-698.
61. Strange B.A., Fletcher P.C., Henson R.N., Friston K.J., Dolan R.J. Segregating the functions of human hippocampus. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:4034-4039.
62. Strange B.A., Witter M.P., Lein E.S., Moser E.I. Functional organization of the hippocampal longitudinal axis. Nat. Rev. Neurosci. 2014, 15:655-669.
63. Tesche C.D., Karhu J. Theta oscillations index human hippocampal activation during a working memory task. Proc. Natl. Acad. Sci. U. S. A. 2000, 97:919-924.
64. van Kesteren M.T., Ruiter D.J., Fernandez G., Henson R.N. How schema and novelty augment memory formation. Trends Neurosci. 2012, 35:211-219.
65. Van Veen B.D., van Drongelen W., Yuchtman M., Suzuki A. Localization of brain electrical activity via linearly constrained minimum variance spatial filtering. IEEE Trans. Biomed. Eng. 1997, 44:867-880.
66. Vinogradova O.S. Hippocampus as comparator: role of the two input and two output systems of the hippocampus in selection and registration of information. Hippocampus 2001, 11:578-598.
67. Yuille A., Kersten D. Vision as Bayesian inference: analysis by synthesis?. Trends Cogn. Sci. 2006, 10:301-308.