More than spikes: Common oscillatory mechanisms for content specific neural representations during perception and memory

Current Opinion in Neurobiology

Volumn 31, Issue , 2015, Pages 33-39

  Watrous, Andrew J ^a   Fell, Juergen ^a   Ekstrom, Arne D ^c,d   Axmacher, Nikolai ^a,b  

^a UNIVERSITY OF BONN   (Germany)

^b GERMAN CENTER FOR NEURODEGENERATIVE DISEASES DZNE   (Germany)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN DEPTH STIMULATION; ELECTROENCEPHALOGRAM; EPISODIC MEMORY; HUMAN; LOCAL FIELD POTENTIAL; MEMORY CONSOLIDATION; NERVE EXCITABILITY; NERVE POTENTIAL; OSCILLATION; PERCEPTION; PRIORITY JOURNAL; REVIEW; SENSORY MEMORY; SIGNAL DETECTION; SIGNAL PROCESSING; SPIKE WAVE; STIMULUS RESPONSE; SYNAPTIC TRANSMISSION; AUDITORY CORTEX; AUDITORY STIMULATION; BRAIN ELECTROPHYSIOLOGY; BRAIN FUNCTION; MENTAL PERFORMANCE; NERVE CELL MEMBRANE POTENTIAL; NERVE CONDUCTION; NEUROBIOLOGY; NEUROMODULATION; NEUROPHYSIOLOGY; NEUROPSYCHOLOGY; NONHUMAN; PERCEPTIVE DISCRIMINATION; RECALL; VISUAL CORTEX; VISUAL STIMULATION; ACTION POTENTIAL; ANIMAL; BIOLOGICAL RHYTHM; MEMORY; NERVE CELL; PHYSIOLOGY;

ACTION POTENTIALS; ANIMALS; BIOLOGICAL CLOCKS; HUMANS; MEMORY; NEURONS; PERCEPTION;

EID: 84906057299     PISSN: 09594388     EISSN: 18736882     Source Type: Journal    
DOI: 10.1016/j.conb.2014.07.024     Document Type: Review

References (65)

1. Schroeder C.E., Wilson D.A., Radman T., Scharfman H., Lakatos P. Dynamics of active sensing and perceptual selection. Curr Opin Neurobiol 2010, 20:172-176.
2. Giraud A.L., Poeppel D. Cortical oscillations and speech processing: emerging computational principles and operations. Nat Neurosci 2012, 15:511-517.
3. Fries P. A mechanism for cognitive dynamics: neuronal communication through neuronal coherence. Trends Cognit Sci 2005, 9:474-480.
4. Siegel M., Donner T.H., Engel A.K. Spectral fingerprints of large-scale neuronal interactions. Nat Rev Neurosci 2012, 13:121-134.
5. Fell J., Axmacher N. The role of phase synchronization in memory processes. Nat Rev Neurosci 2011, 12:105-118.
6. Jutras M.J., Buffalo E.A. Synchronous neural activity and memory formation. Curr Opin Neurobiol 2010, 20:150-155.
7. Watrous A.J., Ekstrom A.D. The spectro-contextual encoding and retrieval theory of episodic memory. Front Hum Neurosci 2014, 8:75.
8. Lee H., Fell J., Axmacher N. Electrical engram: how deep brain stimulation affects memory. Trends Cogn Sci 2013, 17:574-584.
9. Mitzdorf U. Current source-density method and application in cat cerebral cortex: investigation of evoked potentials and EEG phenomena. Physiol Rev 1985, 65:37-100.
10. Buzsaki G., Anastassiou C.A., Koch C. The origin of extracellular fields and currents - EEG, ECoG, LFP and spikes. Nat Rev Neurosci 2012, 13:407-420.
11. Ray S., Maunsell J.H. Differences in gamma frequencies across visual cortex restrict their possible use in computation. Neuron 2010, 67:885-896.
12. Anastassiou C., Perin R., Markram H., Koch C. Ephaptic coupling of cortical neurons. Nat Neurosci 2011, 14:217-223.
13. Anastassiou C.A., Montgomery S.M., Barahona M., Buzsaki G., Koch C. The effect of spatially inhomogeneous extracellular electric fields on neurons. J Neurosci 2010, 30:1925-1936.
14. Frohlich F., McCormick D.A. Endogenous electric fields may guide neocortical network activity. Neuron 2010, 67:129-143.
15. Ozen S., Sirota A., Belluscio M.A., Anastassiou C.A., Stark E., Koch C., Buzsaki G. Transcranial electric stimulation entrains cortical neuronal populations in rats. J Neurosci 2010, 30:11476-11485.
16. Helfrich R.F., Schneider T.R., Rach S., Trautmann-Lengsfeld S.A., Engel A.K., Herrmann C.S. Entrainment of brain oscillations by transcranial alternating current stimulation. Curr Biol 2014, 24:333-339.
17. Polanía R., Nitsche M., Korman C., Batsikadze G., Paulus W. The importance of timing in segregated theta phase-coupling for cognitive performance. Curr Biol 2012, 22:1314-1318.
18. Fell J., Staresina B.P., Do Lam A.T., Widman G., Helmstaedter C., Elger C.E., Axmacher N. Memory modulation by weak synchronous deep brain stimulation: a pilot study. Brain Stimulat 2013, 6:270-273.
19. Suthana N., Haneef Z., Stern J., Mukamel R., Behnke E., Knowlton B., Fried I. Memory enhancement and deep-brain stimulation of the entorhinal area. N Engl J Med 2012, 366:502-510.
20. Quiroga R. Concept cells: the building blocks of declarative memory functions. Nat Rev Neurosci 2012, 13:587-597.
21. Kraskov A., Quiroga R., Reddy L., Fried I., Koch C. Local field potentials and spikes in the human medial temporal lobe are selective to image category. J Cognit Neurosci 2007, 19:479-492.
22. Chan A., Baker J., Eskandar E., Schomer D., Ulbert I., Marinkovic K., Cash S., Halgren E. First-pass selectivity for semantic categories in human anteroventral temporal lobe. J Neurosci 2011, 31:18119-18129.
23. Ekstrom A., Viskontas I., Kahana M., Jacobs J., Upchurch K., Bookheimer S., Fried I. Contrasting roles of neural firing rate and local field potentials in human memory. Hippocampus 2007, 17:606-617.
24. Rey H., Fried I., Quian Quiroga R. Timing of single-neuron and local field potential responses in the human medial temporal lobe. Curr Biol 2014, 24:299-304.
25. van Gerven M., Maris E., Sperling M., Sharan A., Litt B., Anderson C., Baltuch G., Jacobs J. Decoding the memorization of individual stimuli with direct human brain recordings. NeuroImage 2013, 70:223-232.
26. Lopour B., Tavassoli A., Fried I., Ringach D. Coding of information in the phase of local field potentials within human medial temporal lobe. Neuron 2013, 79:594-606.
27. Belitski A., Panzeri S., Magri C., Logothetis N., Kayser C. Sensory information in local field potentials and spikes from visual and auditory cortices: time scales and frequency bands. J Comput Neurosci 2010, 29:533-545.
28. Ng B., Logothetis N., Kayser C. EEG phase patterns reflect the selectivity of neural firing. Cerebral Cortex 2013, 23:389-398.
29. Schyns P., Thut G., Gross J. Cracking the code of oscillatory activity. PLoS Biol 2011, 9.
30. Jafarpour A., Horner A., Fuentemilla L., Penny W., Duzel E. Decoding oscillatory representations and mechanisms in memory. Neuropsychologia 2013, 51:772-780.
31. Jacobs J., Kahana M. Neural representations of individual stimuli in humans revealed by gamma-band electrocorticographic activity. J Neurosci 2009, 29:10203-10214.
32. Fell J., Ludowig E., Rosburg T., Axmacher N., Elger C.E. Phase-locking within human mediotemporal lobe predicts memory formation. Neuroimage 2008, 43:410-419.
33. Rutishauser U., Ross I., Mamelak A., Schuman E. Human memory strength is predicted by theta-frequency phase-locking of single neurons. Nature 2010, 464:903-907.
34. Kayser C., Montemurro M., Logothetis N., Panzeri S. Spike-phase coding boosts and stabilizes information carried by spatial and temporal spike patterns. Neuron 2009, 61:597-608.
35. Hyman J., Zilli E., Paley A., Hasselmo M. Working memory performance correlates with prefrontal-hippocampal theta interactions but not with prefrontal neuron firing rates. Front Integrat Neurosci 2010, 4:2.
36. Canolty R., Ganguly K., Kennerley S., Cadieu C., Koepsell K., Wallis J., Carmena J. Oscillatory phase coupling coordinates anatomically dispersed functional cell assemblies. Proc Natl Acad Sci U S A 2010, 107:17356-17361.
37. Watrous A.J., Tandon N., Conner C.R., Pieters T., Ekstrom A.D. Frequency-specific network connectivity increases underlie accurate spatiotemporal memory retrieval. Nat Neurosci 2013, 16:349-356.
38. Gross J., Hoogenboom N., Thut G., Schyns P., Panzeri S., Belin P., Garrod S. Speech rhythms and multiplexed oscillatory sensory coding in the human brain. PLoS Biol. 2013, 11.
39. Voytek B., Canolty R.T., Shestyuk A., Crone N.E., Parvizi J., Knight R.T. Shifts in gamma phase-amplitude coupling frequency from theta to alpha over posterior cortex during visual tasks. Front Hum Neurosci 2010, 4:191.
40. Benchenane K., Tiesinga P., Battaglia F. Oscillations in the prefrontal cortex: a gateway to memory and attention. Curr Opin Neurobiol 2011, 21:475-485.
41. Akam T., Kullmann D. Oscillatory multiplexing of population codes for selective communication in the mammalian brain. Nat Rev Neurosci 2014.
42. Panzeri S., Brunel N., Logothetis N., Kayser C. Sensory neural codes using multiplexed temporal scales. Trends Neurosci 2010, 33:111-120.
43. Cabral H., Vinck M., Fouquet C., Pennartz C., Rondi-Reig L., Battaglia F. Oscillatory dynamics and place field maps reflect hippocampal ensemble processing of sequence and place memory under NMDA receptor control. Neuron 2014, 81:402-415.
44. Ekstrom A.D., Watrous A.J. Multifaceted roles for low-frequency oscillations in bottom-up and top-down processing during navigation and memory. Neuroimage 2014, 85 Pt 2:667-677.
45. Siegel M., Warden M., Miller E. Phase-dependent neuronal coding of objects in short-term memory. Proc Natl Acad Sci U S A 2009, 106:21341-21346.
46. Jacobs J., Kahana M., Ekstrom A., Fried I. Brain oscillations control timing of single-neuron activity in humans. J Neurosci 2007, 27:3839-3844.
47. van der Meij R., Kahana M., Maris E. Phase-amplitude coupling in human electrocorticography is spatially distributed and phase diverse. J Neurosci 2012, 32:111-123.
48. Jacobs J., Lega B., Anderson C. Explaining how brain stimulation can evoke memories. J Cognit Neurosci 2012, 24:553-563.
49. Fuentemilla L., Penny W.D., Cashdollar N., Bunzeck N., Duzel E. Theta-coupled periodic replay in working memory. Curr Biol 2010, 20:606-612.
50. Lisman J.E., Jensen O. The theta-gamma neural code. Neuron 2013, 77:1002-1016.
51. Buzsaki G. Neural syntax: cell assemblies, synapsembles, and readers. Neuron 2010, 68:362-385.
52. Tort A.B., Komorowski R.W., Manns J.R., Kopell N.J., Eichenbaum H. Theta-gamma coupling increases during the learning of item-context associations. Proc Natl Acad Sci U S A 2009, 106:20942-20947.
53. Benchenane K., Peyrache A., Khamassi M., Tierney P.L., Gioanni Y., Battaglia F.P., Wiener S.I. Coherent theta oscillations and reorganization of spike timing in the hippocampal-prefrontal network upon learning. Neuron 2010, 66:921-936.
54. Kendrick K.M., Zhan Y., Fischer H., Nicol A.U., Zhang X., Feng J. Learning alters theta amplitude, theta-gamma coupling and neuronal synchronization in inferotemporal cortex. BMC Neurosci 2011, 12:55.
55. Wimber M., Maass A., Staudigl T., Richardson-Klavehn A., Hanslmayr S. Rapid memory reactivation revealed by oscillatory entrainment. Curr Biol 2012, 22:1482-1486.
56. Jutras M.J., Fries P., Buffalo E.A. Oscillatory activity in the monkey hippocampus during visual exploration and memory formation. Proc Natl Acad Sci U S A 2013, 110:13144-13149.
57. Rizzuto D.S., Madsen J.R., Bromfield E.B., Schulze-Bonhage A., Kahana M.J. Human neocortical oscillations exhibit theta phase differences between encoding and retrieval. Neuroimage 2006, 31:1352-1358.
58. Axmacher N., Mormann F., Fernandez G., Elger C.E., Fell J. Memory formation by neuronal synchronization. Brain Res Rev 2006, 52:170-182.
59. Canolty R.T., Ganguly K., Carmena J.M. Task-dependent changes in cross-level coupling between single neurons and oscillatory activity in multiscale networks. PLoS Comput Biol 2012, 8:e1002809.
60. Salazar R., Dotson N., Bressler S., Gray C. Content-specific fronto-parietal synchronization during visual working memory. Science 2012, 338:1097-1100.
61. Majima K., Matsuo T., Kawasaki K., Kawai K., Saito N., Hasegawa I., Kamitani Y. Decoding visual object categories from temporal correlations of ECoG signals. Neuroimage 2014, 90:74-83.
62. Manning J.R., Sperling M.R., Sharan A., Rosenberg E.A., Kahana M.J. Spontaneously reactivated patterns in frontal and temporal lobe predict semantic clustering during memory search. J Neurosci 2012, 32:8871-8878.
63. Cohen M.X. Fluctuations in oscillation frequency control spike timing and coordinate neural networks. J Neurosci 2014, 34:8988-8998.
64. Panagiotides H., Freeman W.J., Holmes M.D., Pantazis D. Behavioral states may be associated with distinct spatial patterns in electrocorticogram. Cogn Neurodyn 2011, 5:55-66.
65. Hanslmayr S., Staudigl T., Fellner M.C. Oscillatory power decreases and long-term memory: the information via desynchronization hypothesis. Front Hum Neurosci 2012, 6:74.