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Modulation of theta phase sync during a recognition memory task

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  • 1. Cognitive neuroscience and neuropsychology 1Modulation of theta phase synchronization in the humanelectroencephalogram during a recognition memory taskSung-Phil Kima, Jae-Hwan Kanga, Seong-Hyun Choea, Ji Woon Jeongb,Hyun Taek Kimb, Kyongsik Yunc, Jaeseung Jeongc and Seung-Hwan LeedTo the extent that recognition memory relies on synchronized between the frontal and the left parietal areasinteractions among widely distributed neural assemblies during the recognition of previously viewed objects. Theseacross the brain, phase synchronization between brain results suggest that the recognition memory processrhythms may play an important role in meditating those may involve an interaction between the frontal andinteractions. As the theta rhythm is known to modulate the left parietal cortical regions mediated by theta phasein power during the recognition memory process, we aimed synchronization. NeuroReport 00:000–000 2012 Wolters cto determine how the phase synchronization of the theta Kluwer Health | Lippincott Williams & Wilkins.rhythms across the brain changes with recognition NeuroReport 2012, 00:000–000memory. Fourteen human participants performed a visualobject recognition task in a virtual reality environment. Keywords: electroencephalogram, phase synchronization, recognition memory, theta oscillations, virtual realityElectroencephalograms were recorded from the scalpof the participants while they either recognized objects that Departments of aBrain and Cognitive Engineering, bPsychology, Korea University, Seongbuk-gu, Seoul, cDepartment of Bio and Brain Engineering, Koreahad been presented previously or identified new objects. Advanced Institute of Science and Technology (KAIST), Daejeon and dFrom the electroencephalogram recordings, we analyzed Department of Psychiatry, Ilsan Paik Hospital, Inje University, Goyang, Gyeonggi, Republic of Koreathe phase-locking value of the theta rhythms, whichindicates the degree of phase synchronization. We found Correspondence to Seung-Hwan Lee, MD, PhD, Department of Psychiatry, Ilsan Paik Hospital, Inje University, 2240 Daehwa-dong, Ilsan seo-gu, Goyang,that the overall phase-locking value recorded during Gyeonggi 411-706, Republic of Koreathe recognition of previously viewed objects was greater Tel: + 82 319 107 260; fax: + 82 319 199 776; e-mail: lshspss@hanmail.netthan that recorded during the identification of new objects.Specifically, the theta rhythms became strongly Received 26 March 2012 accepted 10 April 2012Introduction retrieval of recognition memories [7,8]. The cross-correla-Recognition memory, which is a complex cognitive func- tion of theta and gamma oscillations between the frontaltion, requires communication between neural assemblies and the parietal cortical regions became stronger withover the brain [1]. This neural communication induces recognition memory [9]. Increases in frontoparietal coher-local and global temporal alignments of the firing activity ence in gamma oscillations were also induced by recogni-of neural assemblies [2,3]. It also induces the modulation of tion memory [10].the brain oscillations reflecting synchronous activity of a Phase synchronization in the human EEG has also beenneural assembly; the amplitude of an oscillation indicates associated with recognition memory [2,11]. However,the modulation of a local neural assembly, whereas phase although many studies have reported the modulation ofsynchronization between oscillations reflects synchronous gamma phase synchronization between the frontal andfiring activity between assemblies [3]. Especially, there is the parietal cortical regions in the context of recognitionsubstantial evidence that phase synchronization is a key memory [4,10], little is known about how theta phasemechanism underlying neural communication [2]. synchronization is modulated relative to recognitionThe modulation of phase synchronization across distrib- memory.uted brain regions has been associated with many cogni- Therefore, we aim to investigate the patterns of thetative functions [3] as well as memory processes [4]. Phase phase synchronization in the human EEG during a recogni-synchronization during memory retrieval has primarily tion memory task. The previous findings lead us to predictbeen examined with theta and gamma oscillations. The that theta phase synchronization across the frontal androle of gamma oscillations is to bind diverse perceptual parietal cortical regions increases during recognition memory.information into memory, whereas the role of theta In agreement with a previous study [12], we also expect theoscillations is to control the temporal order of individual left parietal area to be a focal point in theta synchronizationmemory representations [1,5,6]. networks.A number of studies have reported theta and gammaoscillations in the human electroencephalogram (EEG) in Participants and methodsthe context of recognition memory [1]. The power of Fourteen healthy individuals (five men, nine women,theta and gamma oscillations increased with the successful 29.2±6.8 years old) participated in the study. All of the0959-4965 2012 Wolters Kluwer Health | Lippincott Williams & Wilkins c DOI: 10.1097/WNR.0b013e328354afedCopyright © Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
  • 2. 2 NeuroReport 2012, Vol 00 No 00 participants provided written informed consent. The EEG recording and acquisition were performed using the experimental procedure was approved by the Ethics Neuroscan SynAmps 64-channel amplifier and Quickcap Committee of Inje University (IB-0802-006). All the electrodes (Compumedics Neuroscan Inc., El Paso, Texas, participants had normal or corrected-to-normal vision and USA). The vertical electrooculogram was monitored using no history of neurological disease. The participants per- two electrodes, one placed near the outer canthus of the formed a recognition memory task designed in a virtual left eye and the other beneath the eye. All the scalp environment (VE) [13]. The VE consisted of four locations electrodes were referred to linked electrodes placed (office, library, lounge, and conference room) and each on the left and right earlobes. The impedances were location contained 15 different office items (e.g. a maintained below 10 kO. The analog EEG signals were vending machine in the lounge). The levels of familiarity, sampled at 1 kHz and filtered through both a band-pass emotional valence, and arousal of these items were filter (0.1–100 Hz) and a (60 Hz) notch filter. As we evaluated in a previous study [14]. examined whole-brain EEG synchronizations, we selected 19 channels according to the 10–20 international system Figure 1 illustrates the overall experimental procedure. for analysis. The experiment included a navigation (encoding) session We analyzed 1700 ms segments from each trial: from and a retrieval session. In the navigation session, the par- 500 ms before to 1200 ms after stimulus onset. A total of ticipants passively navigated through the four locations in 520 REC and 458 CR trials from all the participants were a random order. The participants were instructed to included in the analysis, with 37.1±10.5 (average±SD) remember the items in each location. Each object was REC and 32.7±3.5 CR trials per participant. We reduced presented for 2000 ms with an interstimulus interval of noise by removing hidden noise sources using an inde- 5000 ms. In the retrieval session, the participants perfor- pendent component analysis [15]. med a recognition memory task. The participants were instructed to press one button if they recognized an item The EEG signal in each trial was band-pass filtered as having been presented during navigation in the same (4–8 Hz) to extract theta activity using a finite-impulse location (‘old’ items) or the other button if they did not response filter (length: 300 ms; bandwidth: 2 Hz). The recognize the item as having been presented previously instantaneous phase and amplitude of a theta rhythm (‘new’ items). A total of 40 new and 60 old objects were were estimated using the Hilbert transform [16]. The presented for 500 ms each, with randomly varying inter- phase-locking value (PLV) was computed between theta trial intervals (2000–4000 ms). The EEG was recorded rhythms from every pair of EEG channels [17]. The PLV during the retrieval session. We selected those retrieval was the normalized length of the vector sum of unit trials in which the participants correctly recognized old vectors, where the angle of each unit vector represented a items [hereafter called recognition (REC) trials] or cor- phase difference between two rhythms at a given time rectly rejected new items [correct rejection (CR) trials] instant in the corresponding trial. A larger PLV indicates for further analysis. stronger phase synchronization. Fig. 1 (a) Navigation (b) Retrieval Old item Fixation OR Response period New item period Location Item + 2000−4000 ms 500 ms 2000 ms Illustration of the experimental procedure. (a) The virtual environment, with an item in a location as presented during the navigation session (top). During this session, participants passively navigated through a virtual environment containing four locations (library, office, lounge, and meeting room) (bottom). In each of the four locations, 15 items were presented for 2 s each, with an interstimulus interval of 5 s. (b) The retrieval session procedure. In each trial of this session, participants fixed their gaze at a ‘ + ’ mark in the center of the screen for 2-4 s. An item was then presented in one of the four locations for 0.5 s. This item had either been presented in the preceding navigation session (old items) or was newly presented (new items). Participants responded to each item by pressing one of two buttons to identify that item as old or new.Copyright © Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
  • 3. Theta phase synchrony for recognition Kim et al. 3The PLV difference between REC and CR was calculated those for CR from 400 to 1200 ms after stimulus [t(170) >by subtracting the CR PLVs from the REC PLVs and by 2.8, P < 0.01] (Fig. 2b).time-averaging those differences in each nonoverlapping Figure 3 shows the EEG pairs that showed significantpoststimulus window of 100 ms. From all channel pairs, increases in PLVs for either REC or CR (P < 0.01,this yielded 171 PLV difference values for each window. Bonferroni’s) after stimulus onset. The number of pairsWe statistically evaluated whether this set of differences indicating greater PLVs for REC than for CR began towas significantly different from zero using a t-test. Fol- increase at 400 ms after stimulus and peaked in thelowing the same procedure, but replacing PLV with the 900–1000 ms window (Fig. 3a). In contrast, only a fewtrial-average theta amplitude, we also evaluated the dif- electrode pairs indicated greater PLVs for CR than forference in theta amplitude between REC and CR. REC in any of the poststimulus windows.We next investigated pair-wise event-related changes in To further analyze inter-regional phase synchronizationthe PLV difference. Given a pair of the EEG channels, we patterns from the above results, we selected four regionalcompared the 100 PLV difference values in each post- groups of EEG channels: left frontal (LF: FP1, F7, F3),stimulus window with a baseline. The baseline difference right frontal (RF: FP2, F8, F4), left posterior (LP: P7, P3,value was obtained from the 500 ms segment recorded O1), and right posterior (RP: P8, P4, O2). Then, webefore stimulus onset. Using the same procedure as des- calculated the average number of synchronized pairscribed above, we obtained 500 baseline PLV difference between two regions for 0–500 ms after stimulus (beforesamples. The adjusted confidence intervals (CIs) of the stimulus offset) and for 500–1200 ms after stimulus (afterbaseline and the poststimulus window were estimated stimulus offset). We found the strongest phase synchroni-using the bootstrap method (significance level of 0.01) zation between the right frontal and left posterior regions[18]. If the lower bound of the poststimulus CI was for REC during the second period, with an average ofgreater than the upper bound of the baseline CI, we 2.14 synchronized pairs (Fig. 4a). In contrast, less syn-considered the REC PLV to be significantly greater than chronized pairs were observed for CR (Fig. 4b).the CR PLV. In the opposite case, the CR PLV wasconsidered to be significantly greater than the REC PLV. Discussion Recognition in episodic memory involves the retrieval ofResults an event along with other contextual aspects of the event,Of all 14 participants, the average correct response rates including information about time and space, self-reference,were 72.9±14.8% for old items and 95.9±3.5% for new emotional experience, and personal significance [19]. How-items. The reaction times after stimulus onset were ever, conventional stimuli used in laboratory studies of1376.1±165.9 ms for REC and 1050.9±150.0 ms for CR. episodic memory do not provide rich contexts for this complex form of recognition memory [20]. The presentOverall, the REC PLV was greater than the CR PLV study partially addressed this problem by using a VE with(Fig. 2a). Specifically, the REC PLV was significantly realistic stimuli where participants could experience agreater than CR PLV during a period of 400–1100 ms after sensation of immersion [13].stimulus [t(170) > 2.8, P < 0.01]. The CR PLV was greateronly for 200–300 ms after stimulus [t(170) < – 2.8, P < Our observation of strong theta phase synchronization0.01]. The theta amplitudes for REC were greater than between the right frontal and left parietal areas is inFig. 2 (a) Phase (b) Magnitude 0.08 0.4 0.06 0.3 Power difference PLV difference 0.04 0.2 0.02 0.1 0 0 −0.02 −0.1 0 500 1000 0 500 1000 Time (ms) Time (ms)(a) Differences in the theta phase-locking values (PLVs) observed during recognition (REC) and during correct rejection (CR). The average PLVdifferences between REC and CR across all 171 electroencephalogram electrode pairs are plotted for each nonoverlapping 100-ms time windowfrom 0–1200 ms after stimulus. A positive difference indicates that the REC PLV is greater than the CR PLV. (b) Differences in theta power observedduring REC and during CR. The same procedure described above for the PLV was used to analyze theta power.Copyright © Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
  • 4. 4 NeuroReport 2012, Vol 00 No 00 Fig. 3 (a) Recognition (b) Correct rejection 0.0–0.1 s 0.1–0.2 s 0.2–0.3 s 0.3–0.4 s 0.0–0.1 s 0.1–0.2 s 0.2–0.3 s 0.3–0.4 s 0.4–0.5 s 0.5–0.6 s 0.6–0.7 s 0.7–0.8 s 0.4–0.5 s 0.5–0.6 s 0.6–0.7 s 0.7–0.8 s 0.8–0.9 s 0.9–1.0 s 1.0–1.1 s 1.1–1.2 s 0.8–0.9 s 0.9–1.0 s 1.0–1.1 s 1.1–1.2 s Temporal variation in the distribution of phase-synchronized electroencephalogram electrode pairs. Black lines indicate pairs of electrodes that showed significantly greater PLVs during the recognition of old items (a) or during the correct rejection of new items (b) in each 100-ms time window from 0 to 1200 ms after stimulus. Fig. 4 but also long-range communication of these with frontal (a) Recognition (b) Correct rejection neural assemblies. Gamma and theta phase synchronizations have been shown LF RF LF RF to play prominent roles in the encoding and retrieval of episodic memory [1]. Gamma phase synchronization sup- 0–0.5 s ports a bottom-up process of local memory representation, whereas theta phase synchronization supports a top-down RP process to organize local assemblies for integrated memory LP RP LP representation [1]. Specifically, theta phase synchroniza- tion between prefrontal and parietal areas supports the ex- ecutive function for frontal top-down control over posterior LF RF regions [4,11,12,21]. Theta oscillations also mediate inter- LF RF actions between the hippocampus and the neocortical regions during long-term memory processes [22]. Coherent 0.5–1.2 s theta oscillations in a network of prefrontal, mediotempor- al, and visual cortical regions during recognition memory LP RP have been documented using magnetoencephalography [21]. LP RP The modulation of theta phase synchronization observed in the present study may support this theoretical role of theta Inter-regional theta phase synchronization patterns. The phase-locking phase synchronization in frontal top-down control over value (PLV) was used to measure the connectivity between the left posterior cortical regions during the retrieval of recognition frontal (LF), right frontal (RF), left parietal (LP), and right parietal (RP) regions of the scalp during the retrieval of recognition memory of old memory. items (a) and during the correct rejection of new items (b). Inter-regional connectivity was analyzed for two poststimulus time segments: Our results indicated that theta phase synchronization and 0–500 ms (while items were visible) and 500–1200 ms (after items had disappeared). The thickness of each line is proportional to the average amplitude increased during the recognition of old items number of cross-region pairs of electrodes that showed significant approximately 400 ms after stimulus onset. In previous increases in PLV. The maximum thickness corresponds to 2.14 pairs (per 100 ms) and the minimum thickness corresponds to 0.14. ERP studies, this period was associated with the recol- lection process [23]. It has also been shown that theta power increases significantly during a recollection period of 600–1200 ms, indicating that induced theta oscillations agreement with the previous neuroimaging results of the may reflect neural mechanisms underlying recollection effects of recognition. A meta-analysis of functional MRI [8]. Note that the present study examined changes in studies showed that the loci of such effects were theta synchronizations during the recognition of old and concentrated in the left parietal area [12]. Our results new objects without further distinguishing between famil- suggest that the recognition memory process involves not iarity and recollection of recognition memory, as it focused on only the local activation of left parietal neural assemblies the two cases in which participants recognized either an oldCopyright © Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
  • 5. Theta phase synchrony for recognition Kim et al. 5item in its previous location or that a completely new item. 5 Miltner WH, Braun C, Arnold M, Witte H, Taub E. Coherence of gamma-bandAlthough we did not examine how theta activity would EEG activity as a basis for associative learning. Nature 1999; 397: 434–436.change if the participants recognized old items in new 6 Lee SH, Kim DW, Kim EY, Kim S, Im CH. Dysfunctional gamma-band activitylocations, answering this latter question would be helpful for during face structural processing in schizophrenia patients. Schizophr Resunderstanding how phase synchronization supports familiar- 2010; 119:191–197. 7 Klimesch W, Doppelmayr M, Yonelinas A, Kroll NE, Lazzara M, Rohm D, et al.ity and recollection. A further study will address this question Theta synchronization during episodic retrieval: neural correlates ofto determine whether dual recognition memory processes conscious awareness. Brain Res Cogn Brain Res 2001; 12:33–38. 8 ¨ Gruber T, Tsivilis D, Giabbiconi CM, Muller MM. Inducedwould induce distinct phase synchronization patterns. electroencephalogram oscillations during source memory: familiarity is reflected in the gamma band, recollection in the theta band.Conclusion J Cogn Neurosci 2008; 20:1043–1053. 9 Burgess AP, Ali L. Functional connectivity of gamma EEG activityThis study documented an increase in theta phase is modulated at low frequency during conscious recollection.synchronization during recognition memory. The results Int J Psychophysiol 2002; 46:91–100.suggest that theta phase synchronization may be impor- 10 Summerfield C, Mangels JA. Functional coupling between frontal and parietal lobes during recognition memory. NeuroReport 2005; 16:117–122.tant in integrating widespread recognition memory traces. 11 Klimesch W, Freunberger R, Sauseng P, Gruber W. A short review of slowStrong theta phase synchronizations were found between phase synchronization and memory: evidence for control processes inthe right frontal and the left parietal regions, which may different memory systems? Brain Res 2008; 1235:31–44. 12 Vilberg KL, Rugg MD. Memory retrieval and the parietal cortex: a reviewreflect large-scale functional connectivity between these of evidence from a dual-process perspective. Neuropsychologia 2008;regions during recognition memory processes. 46:1787–1799. 13 Kim YY, Kim HJ, Kim EN, Ko HD, Kim HT. Characteristic changes in the physiological components of cybersickness. Psychophysiology 2005;Acknowledgements 42:616–625.This work was supported by the National Research 14 Hahm J, Lee K, Lim SL, Kim SY, Kim HT, Lee JH. Effects of active navigationFoundation (NRF) of Korea Grant funded by the Korean on object recognition in virtual environments. Cyberpsychol Behav 2007; 10:305–308.Government (NRF-2010-32A-B00282). S.P.K., J.H.K., and 15 Makeig S, Bell AJ, Sejnowski TJ. Independent component analysis ofS.H.C. were also supported by World Class University electroencephalographic data. Adv Neural Inf Process Syst 1996; 8:(WCU) program (R31-10008) and the Basic Science 145–151. 16 Bruns A. Fourier-, Hilbert- and wavelet-based signal analysis: are they reallyResearch Program (2011-0026502) of the NRF of Korea different approaches? J Neurosci Methods 2004; 137:321–332.funded by the Ministry of Education, Science and 17 Lachaux JP, Rodriguez E, Martinerie J, Varela FJ. Measuring phase synchronyTechnology. in brain signals. Hum Brain Mapp 1999; 8:194–208. 18 Payton ME, Greenstone MH, Schenker N. Overlapping confidence intervals or standard error intervals: what do they mean in terms of statisticalConflicts of interest significance? J Insect Sci 2003; 3:34.There are no conflicts of interest. 19 Piefke M, Fink GR. Recollections of one’s own past: the effects of aging and gender on the neural mechanisms of episodic autobiographical memory. Anat Embryol (Berl) 2005; 210:497–512.References 20 Burgess N, Maguire EA, Spiers HJ, O’Keefe J. A temporoparietal and1 Nyhus E, Curran T. Functional role of gamma and theta oscillations in prefrontal network for retrieving the spatial context of lifelike events. episodic memory. Neurosci Biobehav Rev 2009; 34:1023–1035. NeuroImage 2001; 14:439–453.2 Womelsdorf T, Schoffelen JM, Oostenveld R, Singer W, Desimone R, 21 ¨ Guderian S, Duzel E. Induced theta oscillations mediate large-scale Engel AK, et al. Modulation of neuronal interactions through neuronal synchrony with mediotemporal areas during recollection in humans. synchronization. Science 2007; 316:1609–1612. Hippocampus 2005; 15:901–912.3 Varela F, Lachaux JP, Rodriguez E, Martinerie J. The brainweb: phase 22 Zion-Golumbic E, Kutas M, Bentin S. Neural dynamics associated with synchronization and large-scale integration. Nat Rev Neurosci 2001; 2: semantic and episodic memory for faces: evidence from multiple 229–239. frequency bands. J Cog Neurosci 2010; 22:263–277.4 Fell J, Axmacher N. The role of phase synchronization in memory processes. 23 Curran T, Cleary AM. Using ERPs to dissociate recollection from familiarity Nat Rev Neurosci 2011; 12:105–118. in picture recognition. Brain Res Cogn Brain Res 2003; 15:191–205.Copyright © Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.

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