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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 3 rd 4 th 2008 Slide 2 (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 Oscillations and the control of information processing: Outline of the structure of argumentation and proposed hypotheses Slide 3 Part 1.1 Timing of neuronal activity and information processing Slide 4 Inhibition Minimum Maximum Time Cell 2 Cell 1 Cell 3 Cell 1 Cell 2 Cell 3 Excitation (Pyramidal cells) Maximum Minimum 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. Basics: Inhibition, Excitation and Timing Slide 5 Large amplitudes tend to entrain many neurons Inhibition Minimum Maximum Time Cell 2 Cell 1 Cell 3 Cell 1 Cell 2 Cell 3 Excitation (Pyramidal cells) Maximum Minimum Basics: Inhibition, Amplitude and Timing Slide 6 Example 1: Alpha-like oscillations control the timing of sensory coding Nicolelis & Fanselow, (2002). Thalamcortical optimization of tactile processing according to behavioural state. Nature Neurosci. 5 (6), 517-523. Whisker movement a) Top-down control of sensory encoding during exploratory behavior b) c) Slide 7 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. Example 2: Alpha oscillations and the timing of information processing Hz Theta Lower-1 Lower-2 Upper 4 6 8 10 12 Hz 4 6 8 10 12 Hz 4 6 8 10 12 IAF B) Subject with slow alpha at 7.5 Hz A) Average alpha frequency in a large sample of subjects is at about 10 Hz C) Subject with fast alpha at 13.5 Hz Range of variation Power/Amplitude Slide 8 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. Hz 10 5 + + + + + A)B) Age (years) Alzheimer (65 years) Young Adults (25 Years) 1 2 3 4 5 6 7 8 9 11 13 15203040506070 Hz 10 5 Age (A) and performance related (B) differences in IAF IAF increases and declines with age just as processing speed, cognitive performance and brain volume does Good memory performers Bad memory performers Example 2: Alpha oscillations and the timing of information processing Slide 9 Part 1.2 Oscillations and the spatio-temporal organisation of information processing Slide 10 First half retention interval Second half retention interval Manipulation Retention Upper alpha phase coherence: leading and trailing sites 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. Slide 11 Part 2 Slow frequency oscillations: Conscious control of information processing. The functional meaning of theta and alpha Slide 12 (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 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 : Slide 13 ERD% ERS% 50 0 50 100 -1000 -500 0 500 1000 ms Picture encoding (hits, dotted) and recognition (hits, bold; correct rejections dashed ). O1; IAF = 10.3 ERD% ERS% 50 0 50 100 A) Theta; 4.3-6.3HzB) Lower-1 alpha; 6.3-8.3 Hz ERD% ERS% 50 0 50 100 ERD% ERS% 50 0 50 100 C) Lower-2 alpha; 8.3-10.3 Hz D) Upper alpha; 10.3-12.3 Hz Theta old/new - effect Evoked theta; recogn. hits Evoked lower-2 alpha; recogn. hits Evoked lower-1 alpha; recogn. hits Evoked upper alpha; recogn. hits -1000 -500 0 500 1000 ms 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. Slide 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. Theta ERS Evoked theta 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. Slide 15 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 16 56 sec 25 items Lag 8 28 sec 15 items Lag 2 7 sec Retrieval from Retrieval from WMintermediate memory Block 1 Block 2.. Block 8 Continous Word Recognition Paradigm 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. Slide 16 ms -200.0-100.00.0100.0200.0300.0400.0500.0600.0700.0800.0 V 0.0 -2.5 -5.0 2.5 5.0 ms -200.0-100.00.0100.0200.0300.0400.0500.0600.0700.0800.0 V 0.0 -2.5 -5.0 2.5 5.0 Po3 Pz 1 st presentation Lag 16 Lag 8 Lag 2 ms -200.0-100.00.0100.0200.0300.0400.0500.0600.0700.0800.0 V 0.0 -2.5 -5.0 2.5 5.0 O1 P3P2 N2 N1 P1 Slide 17 Evozierte Power Lag2Evozierte Power Lag16 ERD Lag2ERD Lag16 Whole power Lag2Whole Power Lag16 PLI Lag2PLI Lag16 Differenzmaps fr Eletrode T5 Evoked Theta Theta ERS Alpha ERD Theta Phase Locking Slide 18 Slide 19 Evoked theta in P2 time window (around 300 ms) Low resolution electromagnetic tomography LORETA (Pascual-Marqui et al., 1994) Slide 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 1.1 0.8 0.5 0.2 0 z-values Theta reading task semantic task Upper alpha reading task semantic task *** reading > semantic 1.11.2 2.1 3.1 4.1 2.2 3.2 4.2 1.11.2 2.1 3.1 4.1 2.2 3.2 4.2 n.s * reading < semantic ** reading < semantic *** reading < semantic 3rd chunk retrieval of super- ordinate concept in semantic task Evidence for hypothesis that semantic memory is related to upper alpha ERD Significant 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. 1. chunk 2. chunk 3. chunk 4. chunk Theta ERS and Upper Alpha ERD scaled in red Slide 33 Part 2.2.2 Alpha and Perception No ERD but phase locking during re-activation of a trace 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. 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). Slide 34 Mean reaction time ~ 500 ms 0.5 1 1.5 Power bad -0.500.5 5 10 15 20 PLI good -0.500.5 5 10 15 20 0.1 0.2 0.3 0.4 PLI bad -0.500.5 5 10 15 20 Power good -0.500.5 5 10 15 20 Good perception performers Bad perception performers No upper alpha ERD in perception task Are good and bad performers using different strategies of top-down control? Slide 35 Period of 100 ms = 10 Hz Large alpha phase-locking is associated with a large P1 and N1 component in the EEG Slide 36 Memory task 26 10 14 18 Hz Perception task 26 10 14 18 Hz Recording site: Pz Prestimulus alpha synchronization cf Hanslmayr et al. 2006, 207) Prestimulus alpha synchronization may reflect different strategies of top-down control that lead to differences in performance Slide 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 % Correlation between alpha power (8 12 Hz) and detection performance. Both scales are transformed to ranks. prestimulus power (- 500 to 0 ms) Slide 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. Slide 39 Resting condition, eyes open Slide 40 Part 2.2.3 Alpha ERS reflects control of search area/ blocking of retrieval Slide 41 Upper Alpha, Temporal sites, Hits 30 0 60 ERD% ERS% 1000 ms Memory Set Warning signal Probe Load 10, varied Load 5, consistent ENCODING RETENTION RETRIEVAL Cognitive processes: Task sequence: 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 ) Encoding, Load 10 varied Reference Retention, set size 4 Retention, set size 2 Pz Absolute Power 5 10 15 20 2 4 6 8 10 12 14 16 Hz Pz 2 4 6 8 10 12 14 16 Hz Absolute Power 5 10 15 20 Slide 42 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. 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? Suppression of retrieval of items from previous trials helps to reduce interference 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. 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 Slide 43 Part 2.2.4 Alpha phase and top-down control Slide 44 Memory set 500ms Retention Interval 2500ms Probe & Response Match or no match? Retention Manipulation pure retention retention + manipulation (rotation around vertical midline) 2 analysing intervals (0 1000 ms and 1000 - 2000 ms after memory item offset) 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 Slide 45 First half retention interval Second half retention interval Upper Alpha between 9.8 and 12.7 Hz Slide 46 First half retention interval Second half retention interval Manipulation Retention Upper alpha coherence: leading and trailing sites Slide 47 Part 3: Process binding and consciousness Event-related phase reorganization (ERPR) and between frequency phase coupling may reflect binding of different processes that are controlled by consciousness Slide 48 ms -5000500 ms -5000500 ms -5000500 ms Hz -1000-5000500 5 10 15 20 ms Hz -1000-5000500 5 10 15 20 ms Hz -1000-5000500 5 10 15 20 Whole Power Evoked Power PLI F7, set size 4O2, set size 4 logarithmic scale for power PLI Upper Alpha Sync. during retention 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. Slide 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 Slide 50 permutation test (1000 perm.) for PLI at O2 (100-500 ms): tsum=0.022; No univariate sign. diff.: 200-500 ms Difference of phase-locking index at 12 Hz: load 4 load 2 Slide 51 m:n phase synchronization; F7 / O2 Slide 52 ERPs Sternberg yes response, load 2 (blue) and load 4 (red) -2 0 2 4 6 V 85 ms 11.8 Hz 250 500 ms 170 ms 5.9 Hz RT, load 2 400 ms RT, load 4 524 ms P3 -4 -2 0 2 4 V 250 500 ms F7 O2 ERPs generated (in part) by nested theta and upper alpha. Phase reversal between left frontal and right posterior sites. F7 dominated by theta O2 dominated by upper alpha and theta Significant theta and upper alpha PLI and significant phase coupling suggest nested oscillations as illustrated below. Slide 53 P1 N1 Phase locking index Evoked Power Event-related Potential O2 M+M- PLI Gabor wavelet estimate (V) 00.6 20 5 10 5 Hz -10 0 10 V -0.500.51 Time (sec) 0 5 10 15 20 Frequency (Hz) Stimulus Good memory performers (M+) show a significantly larger phase locking in the N1 time window as compared to bad performers (M-) Slide 54 A) Alpha: 10 Hz Sinus 0 50 100 150 200 - + P1 at 100 ms N1 at 150 ms Resetting at 25 ms B) Theta:, 6 Hz Sinus - + N1 at 150 ms Resetting at 24.9 ms 24.9 66.6 108.3 ms P1 0 50 100 150 200 Period = 166.7 ms, 0 50 100 150 200 C) Phase alignment at N1 N1 at 150 ms D) Superposition 0 50 100 150 200 P1 latency is 86 ms N1 at 150 ms Interpeak latency is 150-86 = 64ms 7.8 Hz The basic properties of the P1-N1 complex can be described by a superposition of an evoked theta and alpha wave Slide 55 Part 3.1 Instantaneous Phase Alignment (IPA) between frequencies generates event-related potentials (ERPs) Slide 56 Picture encoding and retrieval task. Data and methods from: Gruber,W., Klimesch, W., Sauseng, P. & Doppelmayr M. (2004). Alpha phase synchronization predicts P1 peak latency and amplitude size. Cerebral Cortex, in press. N1 P1 Time [ms] Voltage [V] Event-related potential a c -500-25002505007501000 0 -10 -20 10 20 Time [ms] Frequency [Hz] Gabor estimates max min Evoked power b d -500-25002505007501000 5 10 15 20 Time [ms] Frequency [Hz] Whole power -500-25002505007501000 5 10 15 20 Time [ms] Frequency [Hz] Significant PLI ( = 10 %) -500-25002505007501000 5 10 15 20 Sign. PLI min max n.s. Gabor estimates max min Recording site O1, example for one subject Slide 57 Frequency [Hz] P1 N1 Phase angle; pos. peak, neg. peak (1) Test for circular unimodal distribution of the phase angle (Hodges-Ajne test) (2) For selected frequencies at each time point the mean phase angle was determined. Steps for determining a significant phase alignment between frequencies (for each time point and frequency bin): (3) By using confidence intervals it was tested whether the phase angle of each selected frequency bin deviates significantly from mean phase angle. (4) From all selected cases only those with a significant increase in PLI were considered. Phase alignment between frequencies, example for one subject (data from Gruber et al. 2004) e Slide 58 h Phase alignment and ERP over all subjects Circular histogram of phase angle at P1 / N1 counts 0 1 P1 N1 0 90 180 270 30 60120 150 210 240 300 330 g Time [ms] Frequency [Hz] pos. peak (360) neg. peak (180) pos. going neg. going pos. goingneg. going Sign. phase alignment ERP [V] -20 +20 5 10 15 20 40 80120160 200 240 f pos. peak (0) Slide 59 Timet1 t2t3 Prestimulus Stimulus Poststimuus Theta Upper Alpha Phase reset Phase reset Co-activation of both networks: Information exchange? Slide 60 Part 3.2 The P1 may reflect alpha-ERPR Hypothesis: The P1 is the earliest manifestation of a top-down process during early sensory processing in sensory-semantic long-term memory which is functionally associated with alpha activity. The general idea is that under conditions where sensory processing is guided by a specific expectancy e.g., about the spatial location and/or type of stimulus, the P1 amplitude will be larger than under conditions where specific expectancies are lacking. For a Review see: Klimesch, Sauseng & Hanslmayr (2007). EEG alpha oscillations: The inhibition/timing hypothesis. Brain Research reviews. Slide 61 Degraded picture recognition task; Data analysis in progress Example 1: The P1 is not a sensnory component. It is missing if expectancy/early categorization is missing Recording site Oz Recording site O2 Completely degraded picture Not degraded picture P1 appears graduelly as expectancy becomes more specific Slide 62 The circle represents the stimulus space ~ All possible stimuli that may appear in a particular task/condition. If the P1 is generated by evoked alpha, the P1 should reflect inhibition as alpha does Highly specifc expectancy Specifc expectancyVague expectancy The P1 may be related to the inhibition of access to irrelevant stimuli inhibition Slide 63 Picture categorization task: Objects vs. Scrambled objects Example 2: The P1 may reflect top-down induced inhibition Slide 64 P1 N1 ERP at Oz The average median for the response times for objects was 490.1 ms (SD=0.65 ms) and 506.1 ms for scrambled objects. Difference is not significant. Objects Scrambled Objects Slide 65 Larger evoked alpha for scrambled objects in time window of P1 Slide 66 .. Cue: Arrow, 34 ms; Random SOA (600-800 ms); Target 50 ms The cue indicates the most likely side (p =.75; valid trials). Spatial Cue Paradigm after Posner Hemifield presentation of two targets (short and long bar).. Cue: Arrow, 34 ms; Random SOA (600-800 ms); Target 50 ms VALID Trial, Example: INVALID Trial, Example: Slide 67 Po3Target Valid Ipsi = Target is expected and processed at PO4 Contra = Target is expected and processed at PO3 Po3Target Invalid Ipsi = Target is expected at PO3 but processed at PO4 Contra = Target is expected at PO4 but processed at PO3 Slide 68 Po3 Target VALID Po3 Target INVALID Ipsi = Target is expected and processed at PO4 Contra = Target is expected and processed at PO3 Ipsi = Target expected at PO3 but processed at PO4 Contra = Target expected at PO4 but processed at PO3 100 ms Time course of changes in upper alpha power Slide 69 Example 3: The P1 behaves like a traveling, evoked alpha wave. Slide 70 Table 1 P1 and N1 latencies in ms Component PzP3P4PO3PO4P7P8O1O2 P1138128132120122116108113112 N1183170175166163162159162163 Difference 45 42 43 46 41 46 51 49 51 Stroop task; Klimesch et al 2007 The task is to respond only to ink color but to ignore the meaning of the presented words Slide 71 -40-20020406080100120140160180200220[ms] PO3 -0.5 -1.5 P8 -0.5 -1.5 [V] -40-20020406080100120140160180200220[ms] -0.5 -1.5 [V] O1 -40-20020406080100120140160180200220[ms] -0.5 -1.5 [V] PO4 -40-20020406080100120140160180200220[ms] P4 -0.5 -1.5 [V] -40-20020406080100120140160180200220[ms] -0.5 -1.5 [V] Pz -40-20020406080100120140160180200220[ms] P7 -0.5 -1.5 [V] -40-20020406080100120140160180200220[ms] -0.5 -1.5 [V] P3 -40-20020406080100120140160180200220[ms] -0.5 -1.5 [V] -40-20020406080100120140160180200220[ms] P1 O1 P1 Pz 0 - 16 ms17 - 33 ms33 - 49 ms50 - 66 ms67 - 83 ms84 - 100 ms100 - 116 ms117 - 133 ms134 - 150 ms151 - 167 ms167 - 183 ms184 - 200 ms Filtered ERP (7 to 10 Hz) Topography of filtered ERP C D Slide 72 2 4 6 8 10 12 14 16 18 20 0 3 -1000-800-600-400-2000200400600 800 ms Hz m/s Mean Travel Speed (m/s) Slide 73 -800-4000400 800 ms 0 0.2 Correlation of Single Trial Phase- differences with P1 Latency B C 2 4 6 8 10 12 14 16 18 20 0 0.2 Correlation of Single Trial Phase- differences with N1 Latency 2 4 6 8 10 12 14 16 18 20 -800-4000400 800 ms Hz Slide 74 Part 4: Conclusions 4. 1. Theta For theta the interpretation appears straight forward: This oscillation appears functionally related to processes in a complex WM-system that operates under direct conscious (top-down) control Slide 75 4.2 Alpha Synchronized (upper) alpha reflects control processes in a complex long-term memory (LTM, or knowledge system) system that may either operate under top-down control or may be running automatically in a default-like mode. An important function of these control processes is to keep us semantically oriented in our environment with respect to its meaning, location and time. The reactivity, topography and functional meaning of alpha is similar to that of posterior parts of a default mode network as proposed by Gusnard & Raichle (2001). Raichle and colleagues assume that activity in the posterior cingulate and precuneus during a baseline state (in which no specific task performance is required) is related to the representation (monitoring) of the world around us. For posterior lateral parts of the default mode network the authors assume a specific role for the monitoring of targets at unfamiliar or unexpected locations. It should be emphasized that the default network plays an important role for consciousness as patient studies with lesions in posterior parts of the default network indicate. Slide 76 Gusnard, D.A. & Raichle, M.E. (2001). Searching for a baseline: Functional imaging and the resting human brain. Nature Reviews Neuroscience, 2, 685-694. Is alpha part of the default mode network? The reactivity, topography and functional meaning of alpha is similar to that of posterior parts of a default mode network. (i) Activity decreases in a variety of different tasks; (ii) Resting activity is larger over posterior brain regions, (iii) Both systems are associated with semantic orientation. The default mode network (Gusnard and Raichle, 2001) Slide 77 Oscillations and joy: Peaks are more enjoyable than troughs