Alpha and theta oscillations: Conscious control of information processing in the human brain?

1. Alpha and theta oscillations: Conscious control of information processing in the human brain? Wolfgang Klimesch University of Salzburg Austria May conference on ‚Consciousness, brain rhythms and the perception-action cycle‘ Memphis, May 3rd – 4th 2008

2. Oscillations and the control of information processing: Outline of the structure of argumentation and proposed hypotheses (1) Oscillations: Timing and spatial organization of information processes. Oscillations provide mechanisms that allow the emergence of spatially and temporally organized firing patterns in neural networks. (2) Slow frequency oscillations: Conscious control of information processing.Slow frequency oscillations in the theta and alpha range (of about 4 – 13.5 Hz) are associated with the top-down control of two large processing systems, a working memory system and a a complex knowledge system, allowing semantic orientation in a constantly changing environment. Theta and alpha oscillations exhibit a variety of different synchronization processes (e.g., amplitude increase, phase coupling, event-related phase reorganization) that reflect different types of control processes and different aspects of the timing of cognitive processes. (3) Process binding and consciousness (4) Conclusions

3. Part 1.1Timing of neuronal activity and information processing

4. Basics: Inhibition, Excitation and Timing Oscillations reflect rhythmic fluctuations of the membrane potential (of the dendritic tree and soma). They have a strong influence on the timing of neural firing.The influence of oscillations depends on the excitatory level of affected cells and on the magnitude of their amplitudes. Cell 1 Cell 2 Excitation (Pyramidal cells) Maximum Minimum Inhibition Minimum Maximum Cell 3 Cell 1 Cell 2 Cell 3 Time

5. Basics: Inhibition, Amplitude and Timing Large amplitudes tend to entrain many neurons Cell 1 Cell 2 Excitation (Pyramidal cells) Maximum Minimum Inhibition Minimum Maximum Cell 3 Cell 1 Cell 2 Cell 3 Time

6. Nicolelis & Fanselow, (2002). Thalamcortical optimization of tactile processing according to behavioural state. Nature Neurosci. 5 (6), 517-523. a) Top-down control of sensory encoding during exploratory behavior c) b) Whisker movement b) c) Example 1: Alpha-like oscillations control the timing of sensory coding

7. Example 2: Alpha oscillations and the timing of information processing Individual alpha frequency (IAF) varies to a large degree between subjects (in a range of about 7.5 and 13.5 Hz) and is related to the speed of information processing. This have been shown very early in EEG research: e.g., Surwillo, W. (1961). Frequency of the alpha rhythm, reaction time and age, Nature 191, 823-824. Klimesch, W. (1996). Alpha frequency, reaction time and the speed of processing information, J. Clin. Neurophysiol. 13, 511-518. Range of variation IAF A) Average alpha frequency in a large sample of subjects is at about 10 Hz Power/Amplitude Lower-2  Lower-1  Upper  Theta Hz 4 6 8 10 12 Power/Amplitude B) Subject with slow alpha at 7.5 Hz Hz 4 6 8 10 12 Power/Amplitude C) Subject with fast alpha at 13.5 Hz Hz 4 6 8 10 12

8. Example 2: Alpha oscillations and the timing of information processing Age (A) and performance related (B) differences in IAF Hz Hz A) B) + + 10 10 + + Good memory performers + IAF increases and declines with age just as processing speed, cognitive performance and brain volume does 5 Good memory performers 5 Bad memory performers Bad memory performers Alzheimer (65 years) Young Adults (25 Years) 1 2 3 4 5 6 7 8 9 11 13 15 20 30 40 50 60 70 Age (years) Interindividual differences in alpha frequency vary with age and memory performance. (A) From early childhood to puberty, alpha frequency increases from about 5.5 to more than 10 Hz but then starts to decrease with age. (B) As compared to bad memory performers, good performers have a significantly higher alpha frequency, even in Alzheimer demented subjects.

9. Part 1.2Oscillations and the spatio-temporal organisation of information processing

10. Upper alpha phase coherence: leading and trailing sites Manipulation Retention First half retention interval Second half retention interval Sauseng, P., Klimesch, W., Doppelmayr, M., Pecherstorfer, T., Freunberger, R., Hanslmayr, S., (2005). EEG alpha synchronization and functional coupling during top-down processing in a working memory task. Hum. Brain Mapp. 26, 148-155.

11. Part 2Slow frequency oscillations: Conscious control of information processing. The functional meaning of theta and alpha

12. Part 2.1 Theta Theta appears to be related to different functions of a complex working memory (WM) system. At least two types of task-related responses can be distinguished : (i) A brief phasic event-related increase in theta power probably reflects encoding/retrieval of new (episodic) information. • (ii) A long lasting event-related increase probably reflects top-down control associated with central executive functions. Examples: • The maintenance of information in WM • Spatial navigation (exploratory behavior) • Sustained attention

13. Frequency specificity and functional meaning of theta for episodic encoding. Klimesch et al (2001). Episodic retrieval is reflected by a process specific increase in human theta activity. Neuroscience Letters, 302, 49-52. Picture encoding (hits, dotted) and recognition (hits, bold; correct rejections dashed ). O1; IAF = 10.3 A) Theta; 4.3-6.3Hz B) Lower-1 alpha; 6.3-8.3 Hz Theta old/new - effect ERD% ERS% 50 0 50 100 ERD% ERS% 50 0 50 100 Evoked theta; recogn. hits Evoked lower-1 alpha; recogn. hits -1000 -500 0 500 1000 ms -1000 -500 0 500 1000 ms D) Upper alpha; 10.3-12.3 Hz C) Lower-2 alpha; 8.3-10.3 Hz Evoked lower-2 alpha; recogn. hits Evoked upper alpha; recogn. hits ERD% ERS% 50 0 50 100 ERD% ERS% 50 0 50 100 -1000 -500 0 500 1000 ms -1000 -500 0 500 1000 ms

14. The neural correlates of conscious awareness during successful retrieval are reflected by a late event-related synchronization (ERS) in theta. An early EEG synchronization in the theta band predicted knowing, and a later remembering. Moreover, early and late event-related potentials were also found to predict knowing and remembering, respectively. Klimesch, W., Doppelmayr, M., Yonelinas, A., Kroll, N.E.A., Lazzara, M., Roehm, D., & Gruber, W. (2001). Theta synchronization during episodic retrieval: neural correlates of conscious awareness. Cognitive Brain Research, 12, 33-38. Evoked theta Evoked theta Theta ERS Evoked theta

15. Block 1 Block 2…………….. Block 8 75 words are presented, 45 items are repeated (old), 30 not repeated (new) Yes/no recognition and confidence judgment. Stimulus onset every 3.5 sec 30 items 45 items not repeated repeated (new words) (old words) 15 items Lag 2 7 sec 25 items Lag 8 28 sec 15 items Lag 16 56 sec Retrieval from Retrieval from WM intermediate memory A decaying episodic trace is associated with decreased theta Klimesch, W., Hanslmayr, S., Sauseng, P., Gruber, W., Brozinski, C., Kroll, N.E.A., Yonelinas, A., & Doppelmayr, M. (2006c). Oscillatory EEG correlates of episodic memory trace decay. Cerebral Cortex, 16 (2), 280-290. Continous Word Recognition Paradigm

16. -5.0 -5.0 -2.5 -2.5 µV 0.0 -5.0 µV 0.0 2.5 -2.5 2.5 5.0 µV 0.0 5.0 2.5 -200.0 -100.0 0.0 100.0 200.0 300.0 400.0 500.0 600.0 700.0 800.0 ms 5.0 -200.0 -100.0 0.0 100.0 200.0 300.0 400.0 500.0 600.0 700.0 800.0 ms -200.0 -100.0 0.0 100.0 200.0 300.0 400.0 500.0 600.0 700.0 800.0 1st presentation ms Lag 16 Lag 8 Lag 2 Pz Po3 N2 P2 P3 O1 N1 P1

17. Evoked Theta Theta Phase Locking Evozierte Power Lag2 Evozierte Power Lag16 ERD Lag2 ERD Lag16 Theta ERS Alpha ERD Differenzmaps für Eletrode T5 Whole power Lag2 Whole Power Lag16 PLI Lag2 PLI Lag16

18. Lag effect : Theta , mean over all electrodes 35 Poststimulus Poststimulus Prestimulus Prestimulus intervals intervals , t1 , t1 – – t4 t4 intervals intervals p1, p2 p1, p2 30 25 20 % ERS 15 10 lag lag - - 2 2 lag lag - - 8 8 5 lag lag - - 16 16 0 p1 p1 p2 p2 t1 t1 t2 t2 t3 t3 t4 t4 ( ( - - 400 400 - - - - 200) 200) ( ( - - 200 200 – – 0) 0) (0 (0 – – 200) 200) (200 (200 – – 400) 400) (400 (400 – – 600) 600) (600 (600 – – 800) 800) Lag effect : Theta , T5 35 Poststimulus Poststimulus Prestimulus Prestimulus intervals intervals , t1 , t1 – – t4 t4 intervals intervals p1, p2 p1, p2 30 25 20 % ERS 15 10 lag lag - - 2 2 lag lag - - 8 8 5 lag lag - - 16 16 0 t1 t1 t2 t2 t3 t3 t4 t4 p1 p1 p2 p2 (0 (0 – – 200) 200) (200 (200 – – 400) 400) (400 (400 – – 600) 600) (600 (600 – – 800) 800) ( ( - - 400 400 - - - - 200) 200) ( ( - - 200 200 – – 0) 0)

19. Low resolution electromagnetic tomography LORETA (Pascual-Marqui et al., 1994) Evoked theta in P2 time window (around 300 ms)

20. LORETA (Pascual-Marqui et al., 1994). The P3 component elicited stronger activity for Lag-2 than Lag-16 in left superior temporal gyrus and middle temporal gyrus, posterior cingulated gyrus, bilateral lingual gyrus, and, most interesting, in right hippocampus and parahippocampal gyrus (t > 3.77, p < .05 corrected). There were no significant differences between lag-2 and lag-8, nor between lag-8 and lag-16. LORETA; P3 unfiltered

21. WM comprises an anterior-posterior network Attentional Control/Central executive Phonological loop primarily located in left hemisphere, including - articulatory rehearsal system (BA 44) - temporary STORAGE system (BA 40): ‚Verbal-acoustic‘ STM‘ Visuospatial sketchpad primarily located in right hemisphere, including - frontal areas (BA 6, 47) and - posterior areas (BA, 19, 40): ‚visual STM‘

22. Functional interplay in theta frequency between prefrontal and posterior regions A) character strings B) line drawings From Sarnthein, Petsche, Rappelsberger, Shaw &Von Stein (1998). Synchronization between prefrontal and posterior association cortex during human working memory. PNAS, 95, 7092-7096. Enhanced coherence in the theta range (4-7 Hz) during retention. Connections between electrode sites represent significant increases of coherence above control (P< 0.05 or better). The shaded areas indicate the range of positions of individual electrodes as determined in an MRI study. Note that the occipital electrodes (01, 02) are placed not over primary visual areas, but closer to the parieto-temporo-occipital association region. (a) During retention of character strings in memory, enhanced coherence appeared between prefrontal and posterior cortex. In posterior cortex, the left hemisphere was predominantly involved. (b) coherence- increases during retention of abstract line drawings in memory. Patterns of encanced coherence were similar n both tasks, but more connections appeared in the right hemisphere in the visual task. For convergent evidence see Weiss & Rappelsberger (2000)

23. Is the ‘interplay’ between anterior and posterior regions due to executive functions operating on storage areas? Study by Sauseng, Klimesch, Gruber, Doppelmayr, Stadler, W., & Schabus (2002) Issue of interest: Retrieval processes from LTM (or intermediate memory) activated from WM. Design: Three tasks were performed, a learning, ‘recognition’ and selective retrieval task.First, subjects had to learn a verbal label (numbers between 1-8) for each of a set of 8 abstract pictures. Second, the pictures were presented and subjects had to name the label. Third, in the selective retrieval task, two labels were presented sequentially. Now in response to each label, the respective picture had to be retrieved. To guarantee that subjects are actually retrieving the corresponding pictures they had to perform an imagery task after the presentation of the second label. Label 1 Label 2 Retrieve picture 1 Retrieve picture 2 and perform imagery task

24. ms 0 10 20 30 40 50 60 70 80 90 frontal to occipital Theta - ERP map subject “M“ o x x o x o x 400 x x +1.8 x x µV x 0 x 500 o o x x - 1.8 o o change in direction of theta marked by vertical line o o o x x o 600 o o o o o x x o x x +0.8 x x 700 x x o µV 0 x x - 0.8 o o o o o o x = positive maximum o o 800 o = negative maximum occipital to frontal Evoked theta behaves like a travelling wave. After a label is presented several cycles of theta can be observed travelling from frontal to occipital sites. At about 774 ms (on average) the direction reverses. This ‚latency‘ is correlated with memory performance (number of correct labels in recognition task): r = .39 p < .05.

25. Example of an evoked, ‘traveling’ theta wave, one subject, negative polarity is in blue A Fz Theta-waves single subject “B“ Cz -1.5 po p -1 p+1 Pz -1.0 Oz -0.5 µV 0.0 0.5 1.0 change in direction 1.5 500 600 700 800 900 1000 1100 1200 1300 ms poststim

26. Fz Oz At time of change in direction frontal theta period increases Significant increase in frontal theta period during p0 ms 250 225 200 175 150 * p-1 p-2 po p+1 p+2

27. Upper Alpha Desynchronization (ERBP) over occipital sites as a function of theta reversal Triggered by theta Stimulus triggered Triggered by theta 400 ms

28. Part 2.2 Alpha Part 2.2.1 The key for the functional understanding of alpha: The onset of Alpha ERD reflects retrieval from memory

29. Prepare for encoding: Prepare for retrieval: Do not initiate encoding in WMS Block access to LTMS Control access to LTMS Control encoding into WMS Pre-Stimulus Post-Stimulus Pre-Stimulus Post-Stimulus Memory item Memory item In a conventional, event-related memory task episodic and semantic memory proccesses are required Episodic processing mode: A phasic process concentrated on a specific event Semantic processing mode: A continuous, automatic process ERS Alpha Amplitude Theta Amplitude ERD Time Time

30. Part 2.2.1 The functional dissociation between theta and alpha The behaviour of alpha is puzzling and remarkable in several ways: (i) Whereas other frequencies reliably show an increase in power (event-related synchronization, ERS) in response to a stimulus/event, alpha shows a decrease (event-related desynchronization, ERD) in many tasks. (ii) More recently, it became clear that certain types of tasks reliably elicit alpha ERS. We have suggested recently that the key for understanding alpha is the fact that the onset of upper alpha ERD indicates the onset of access to and retrieval of a trace from LTM (Klimesch et al. 2007).

31. First chunk: subject ‚Ein Hase‘ ,A rabbit Second chunk: finite verb and a reflexive pronoun ,hat sich‘ ‚is‘ Third chunk: object ‚in der Schachtel‘ ‚in the box‘ Fourth chunk: verb ,versteckt‘ ‚hiding‘ ? 800 ms 800 ms 800 ms 800 ms Evidence for hypothesis that semantic memory is related to upper alpha ERDFrom: Röhm, D., Klimesch, W., Haider, H., Doppelmayr, M. (2001). The role of theta and alpha oscillations for language comprehension in the human electroencephalogramm. Neuroscience Letters, 310, 137-140. Experimental design: READING TASK: Subjects were instructed to silently read and to pronounce the sentence right after a question mark would appear. SEMANTIC TASK: Subjects were instructed to read the sentence in order to search a super-ordinate concept for the noun of the third chunk and to pronounce the super-ordinate concept after the question mark appeared. Sample: 22 right handed volunteers (8 males, mean age = 22.88; SD = 3.34; 14 females, mean age = 23.79; SD = 4.41). Each subject had to perform first the reading and then the semantic task.

32. 1.1 0.8 Thetareading task semantic task Upper alphareading task semantic task 0.5 0.2 0 n.s * reading < semantic 1.1 1.2 1.1 1.2 z-values n.s ** reading < semantic 2.1 2.2 2.1 2.2 3rd chunk retrieval of super-ordinate concept in semantic task ** reading < semantic *** reading > semantic 3.1 3.2 3.1 3.2 n.s *** reading < semantic 4.1 4.2 4.1 4.2 Evidence for hypothesis that semantic memory is related to upper alpha ERDSignificant increase in upper alpha ERD during retrieval from semantic long-term memory and semantic processing - although sentences were already presented in the preceding reading task. Theta ERS and Upper Alpha ERD scaled in red 1. chunk 2. chunk 3. chunk 4. chunk

33. Part 2.2.2 Alpha and Perception No ERD but phase locking during ‘re-activation of a trace’ Hanslmayr, S., Klimesch, W., Sauseng, P., Gruber, W., Doppelmayr, M., Freunberger, R., Pecherstorfer, T., 2005. Visual discrimination performance is related to decreased alpha amplitude but increased phase locking. Neurosci. Lett. 375, 64-68. For similar findins see: T. Ergenoglu, T. Demiralp, Z. Bayraktaroglu, M. Ergen, H. Beydagi, Y. Uresin, Alpha rhythm of the EEG modulates visual detection performance in humans, Cognitive Brain Res. 20 (2004) 376-383. These findings were replicated in Hanslmayr et al. (2007). Experimental design: Example of a trial. The subjects were instructed to respond as fast as possible to two target stimuli (p, q) by pressing one of four buttons.

34. PLI good 5 10 15 20 -0.5 0 0.5 No upper alpha ERD in perception task Are good and bad performers using different strategies of top-down control? Good perception performers Bad perception performers Power good Power bad 5 5 1.5 10 10 1 15 15 0.5 20 20 -0.5 0 0.5 -0.5 0 0.5 PLI bad 5 0.4 10 0.3 0.2 15 0.1 20 -0.5 0 0.5 Mean reaction time ~ 500 ms

35. Period of 100 ms = 10 Hz Large alpha phase-locking is associated with a large P1 and N1 component in the EEG

36. Prestimulus alpha synchronization may reflect different strategies of top-down control that lead to differences in performance Prestimulus alpha synchronization Memory task Perception task • 6 10 14 18 Hz • 6 10 14 18 Hz cf Hanslmayr et al. 2006, 207) Recording site: Pz

37. Perceivers (P+) : Group of subjects (n = 15) with a performance that lies significantly above chance (25%). Mean detection rate: 58% Non-Perceivers (P-) : Group of subjects (n = 15) with a performance that is not significantly different from chance. Mean detection rate: 26 % prestimulus power (- 500 to 0 ms) Correlation between alpha power (8 – 12 Hz) and detection performance. Both scales are transformed to ranks.

38. c) For the group of Perceivers (P+), the ongoing prestimulus EEG (- 500 to 0 ms) shows larger phase coupling in trials when subjects failed to perceive the stimulus. d) topography of electrode pairs with larger phase coupling for incorrect as compared to correct responses. e) Number of couplings for each electrode.

39. Resting condition, eyes open

40. Part 2.2.3 Alpha ERS reflects control of search area/ blocking of retrieval

41. Retention, set size 4 Retention, set size 2 Pz Pz Absolute Power 5 10 15 20 Absolute Power 5 10 15 20 Encoding, Load 10 varied Reference 2 4 6 8 10 12 14 16 Hz 2 4 6 8 10 12 14 16 Hz Upper alpha exhibits a load dependent increase in ERS during encoding and retention in memory scanning tasks (Klimesch et al., 1999; Jensen et al., 2002; Schack & Klimesch, 2002; Busch & Herrmann, 2003; Cooper et al., 2003; Herrmann et al., 2004a; Sauseng et al., 2005b) Upper Alpha, Temporal sites, Hits Cognitive processes: ENCODING RETENTION RETRIEVAL Task sequence: Warning signal Memory Set Probe 60 Load 10, varied 30 ERD% ERS% 0 Load 5, consistent 30 1000 ms

42. In a memory scanning task, a subject is in an encoding and retrieval mode. Trial k B 2 H 5 4 L K R 1 F H? Trial k + 1: 3 1 L 4 8 6 R K C 8 F? Interpretation Alpha synchronization reflects inhibitory top-down control to block retrieval of interfering information When the stored memory trace has to be retrieved, however, a strong ERD can be observed. Suppression of retrieval of items from previous trials helps to reduce interference Further Evidence comes from findings about motor behavior and the mu.rhythm: In a study by Hummel et al. (2002) subjects had - in response to visual cues - to perform sequential finger movements on an electrical keybord. The task was either to actually perform the movements (ACT condition) or to look at the cues but to inhibit a response (INH condition). Upper alpha ERD was observed during ACT but ERS during INH The separately performed TMS experiment revealed that the amplitude of the motor evoked potential (MEP) at the hand was reduced during INH as compared to ACT and a baseline condition.

43. Part 2.2.4 Alpha phase and top-down control

44. Sauseng, P., Klimesch, W., Doppelmayr M., Pecherstorfer, T., Freunberger, R., Hanslmayr, S. (2005). EEG alpha synchronization and functional coupling during top-down processing in a working memory task. Human Brain Mapping, in press. Visuo-spatial working memory task Retention pure retention retention + manipulation (rotation around vertical midline) Manipulation 2 analysing intervals (0 – 1000 ms and 1000 - 2000 ms after memory item offset) Memory set 500ms Retention Interval 2500ms Probe & Response Match or no match?

45. Upper Alpha between 9.8 and 12.7 Hz First half retention interval Second half retention interval

46. Upper alpha coherence: leading and trailing sites Manipulation Retention First half retention interval Second half retention interval

47. Part 3: Process binding and consciousnessEvent-related phase reorganization (ERPR)and between frequency phase coupling may reflect binding of different processes that are controlled by consciousness

48. 6 Hz 12 Hz 6 Hz 12 Hz Theta : upper alpha phase coupling in a Sternberg task (load 2 and load 4); Schack, Klimesch & Sauseng (2005). Internat. Journal of Psychophysiology, in press. F7, set size 4 O2, set size 4 5 10 Hz Whole Power Upper Alpha Sync. during retention 15 logarithmic scale for power 20 ms ms -500 0 500 -1000 -500 0 500 5 10 Hz Evoked Power 15 20 ms -500 0 500 ms -1000 -500 0 500 5 PLI PLI 10 Hz 15 20 ms -1000 -500 0 500 -500 0 500 ms

49. Difference of phase-locking index at 6 Hz: load 4 – load 2 permutation test (1000 perm.) for PLI at F7 (0-400 ms): tsum=0.038 no univariate differences

50. Difference of phase-locking index at 12 Hz: load 4 – load 2 permutation test (1000 perm.) for PLI at O2 (100-500 ms): tsum=0.022; No univariate sign. diff.: 200-500 ms