Brain and Cognition 90 (2014) 70–75

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Regional and inter-regional theta oscillation during episodic novelty processing Gwan-Taek Lee a,1, Chany Lee a,1, Kyung Hwan Kim b, Ki-Young Jung c,⇑ a

Department of Neurology, Korea University College of Medicine, 73 Inchon-Ro, Anam-Dong, Seongbuk-Gu, Seoul 136-705, Republic of Korea Department of Biomedical Engineering, College of Health Science, Yonsei University, 234 Maeji-ri, Heungup-myun, Wonju, Gangwon-do, Republic of Korea c Department of Neurology, Seoul National University College of Medicine, 101 Daehak-Ro, Jongno-Gu, Seoul 110-744, Republic of Korea b

a r t i c l e

i n f o

Article history: Accepted 11 June 2014

Keywords: Event-related potentials Recognition Novelty Theta rhythm

a b s t r a c t Recent event-related potential (ERP) and functional magnetic resonance imaging (fMRI) studies suggest that novelty processing may be involved in processes that recognize the meaning of a novel sound, during which widespread cortical regions including the right prefrontal cortex are engaged. However, it remains unclear how those cortical regions are functionally integrated during novelty processing. Because theta oscillation has been assumed to have a crucial role in memory operations, we examined local and inter-regional neural synchrony of theta band activity during novelty processing. Fifteen right-handed healthy university students participated in this study. Subjects performed an auditory novelty oddball task that consisted of the random sequence of three types of stimuli such as a target (1000 Hz pure tone), novel (familiar environmental sounds such as dog bark, buzz, car crashing sound and so on), and standard sounds (950 Hz pure tone). Event-related spectra perturbation (ERSP) and the phase-locking value (PLV) were measured from human scalp EEG during task. Non-parametric statistical tests were applied to test for significant differences between stimulus novelty and stimulus targets in ERSP and PLV. The novelty P3 showed significant higher amplitude and shorter latency compared with target P3 in frontocentral regions. Overall, theta activity was significantly higher in the novel stimuli compared with the target stimuli. Specifically, the difference in theta power between novel and target stimuli was most significant in the right frontal region. This right frontal theta activity was accompanied by phase synchronization with the left temporal region. Our results imply that theta phase synchronization between right frontal and left temporal regions underlie the retrieval of memory traces for unexpected but familiar sounds from long term memory in addition to working memory retrieval or novelty encoding. Ó 2014 Elsevier Inc. All rights reserved.

1. Introduction Episodic novelty is provided by stimuli that are familiar in general but occur in a specific task situation for the first time. Studies of neural processes induced by novelty stimulus have revealed several cognitive stages for response to unexpected environmental change. In the early stage of processing, transient changes in the physical properties of the incoming stimulus are detected, and then attention is captured involuntarily (Friedman, Cycowicz, & Gaeta, 2001). Novelty processing may also be involved in automatic memory retrieval to recognize the meaning of an object

⇑ Corresponding author. Fax: +82 2 2072 7424. E-mail address: [email protected] (K.-Y. Jung). Gwan-Taek Lee and Chany Lee contributed equally as co-first authors to this study. 1

http://dx.doi.org/10.1016/j.bandc.2014.06.009 0278-2626/Ó 2014 Elsevier Inc. All rights reserved.

(Mecklinger, Opitz, & Friederici, 1997; Opitz, Mecklinger, Friederici, & von Cramon, 1999). The functional significance of episodic novelty processing is known to be related to memory encoding and retrieval, based on positron emission tomography (PET) and ERP combined fMRI studies (ERP-fMRI). It is suggested that novelty assessment is subserved by subcortical and temporal as well as parietal cortical regions and novelty encoding is subserved by the frontal lobes (Tulving, Markowitsch, Craik, Habib, & Houle, 1996; Tulving, Markowitsch, Kapur, Habib, & Houle, 1994). Opitz et al. suggested that the superior temporal gyrus is involved in novelty detection, whereas retrieving semantic concepts related to novel sounds additionally engages the right prefrontal cortex (Mecklinger et al., 1997; Opitz et al., 1999), which also showed that the effects of semantic retrieval are depending on the attention on incoming stimulus. The neural mechanisms of novelty processing are reflected in the novelty P3 (Friedman et al., 2001). The novelty P3 has a

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frontocentral distribution, which may be due to engagement of the prefrontal cortex to control sensory-limbic integration (Knight, 1984). However, recent studies suggest that novelty processing involves not only the prefrontal cortex, but also a widespread neural network of cortical regions, including the anterior cingulate gyrus, insula, precentral gyrus, postcentral gyrus, inferior parietal lobule, superior temporal gyrus, cuneus, thalamus, and cerebellum (Strobel et al., 2008). Although most ERP studies using novel stimuli have focused on the mean amplitude and latency of the novelty P3 evoked by the stimulus in a time-locked manner, investigating certain oscillatory characteristics of ERP components may provide additional information compared with that obtained in an averaged ERP analysis (Ko et al., 2012). The theta oscillation may be critical for temporal coding/decoding of active neuronal ensembles and the modification of synaptic weights (Buzsaki, 2002). Theta oscillation is consistently present during memory operations such as working memory (Jensen & Tesche, 2002; Sarnthein, Petsche, Rappelsberger, Shaw, & von Stein, 1998), encoding of new information (Klimesch, 1999), and memory retrieval (Bastiaansen, van der Linden, Ter Keurs, Dijkstra, & Hagoort, 2005; Guderian & Duzel, 2005; Klimesch et al., 2001). It is likely that distinct oscillatory changes in the theta band occur during novelty processing because memory functions are required for processing novel stimuli. Demiralp et al. have reported that the novelty stimulus-evoked P3a component leads to considerable theta activity in distant brain regions (Demiralp, Ademoglu, Comerchero, & Polich, 2001). They interpreted this theta activity as a reaction to rare events that deviate from the stimulus context (Demiralp et al., 2001). However, it remains unclear whether this distant co-activation reflects functional communication of distributed brain regions because functional connectivity between stimulus-relevant cortical regions was not explored. Although local changes in spectral power reflect the synchrony of neuronal activities within a short range, exploring the inter-regional functional connectivity between brain regions presents additional valuable information for the integration of distributed neural activity and this is feasible by observing interregional phase synchronization. Phase-locking synchrony must instead reside in distant connections, either in cortico-cortical fibers or thalamocortical reciprocal pathways (Varela, Lachaux, Rodriguez, & Martinerie, 2001). Further, any mechanism for neural communication must involve interactions between participating local networks (Varela et al., 2001). Thus, both local spectral activity and inter-regional phase synchronization should be evaluated when examining the function of a neuronal network. The aim of the present study was to identify regional and interregional spectral characteristics of EEG during episodic novelty processing in a three-stimulus oddball task. We conducted a single-trial analysis of theta oscillation using event-related spectral perturbation (ERSP) and the phase locking value (PLV) and evaluated specific responses elicited by novelty stimuli in comparison to those by target ones.

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and standard (950 Hz pure tone, p = 0.76, n = 304) sounds. The stimuli duration was 300 ms, and inter-stimulus intervals were varied randomly within 1700–2300 ms. Subjects listened to stimuli delivered through earphones at 65 dB SPL and were instructed to respond only to target stimuli by pushing a button using the right index finger as quickly as possible. Each subject received three blocks of an auditory novelty oddball task containing a mixture of 400 tones. Commercial software (Presentation version 11.0; Neurobehavioral Systems, Inc., Albany, CA, USA) was used to present the stimuli. 2.2. EEG recording EEG was recorded using a 64-channel digital EEG machine (Grass Neurodata Acquisition System, Grass Technologies, Quincy, MA, USA) with an EEG cap with 62 electrodes (Quick-Cap, Compumedics Neuroscan, Charlotte, NC, USA). The reference electrode was set to linked earlobes, impedance was kept below 10 kX, and the band-pass filter setting was set at 0.3–70 Hz with a sampling rate of 1600 Hz. Two electrooculography (EOG) channels (placed on the left and right outer canthi) were added to confirm eyeball movements and to remove EOG artifacts. Participants were seated in a comfortable chair and instructed to continuously focus their eyes on a fixation point on a computer screen. 2.3. Preprocessing and averaged ERP component analysis EEG data was preprocessed using EEGLAB version 10.0b (Delorme & Makeig, 2004) operated under the MATLAB environment (version 7.1, The Mathworks, Natick, MA, USA). After down-sampling (200 Hz), EEG data were epoched between the 800-ms pre-stimulus and 1000-ms post-stimulus time points. Epochs containing waveforms that exceeded ±100 lV were removed by an automated process implemented in EEGLAB. Epochs with remaining artifacts were further eliminated by visual inspection. The mean numbers of epochs included in computations were 97.5 ± 33.1 for target, 91.3 ± 36.9 for novelty, and 887.1 ± 126.4 for standard stimuli. EEG data was re-referenced to the common average reference and bandpass filtered (0.5–30 Hz). For each epoch, a baseline correction was performed using data from 400 ms prior to the stimulus. Independent component analysis (ICA) was applied to correct stereotyped ocular and muscular artifacts. For each subject, the averaged ERP components for each electrode site were obtained. The time window (200–500 ms) was determined by visually inspecting individual waveforms at the midline electrodes (Fz, Cz, and Pz). A positive peak at the Fz electrode within this time window was defined as novelty P3 and, at the Pz electrode, was defined as target P3. Latency was defined for each individual as the point with a maximum positive peak within the time window from the stimulus onset. Amplitude was calculated by averaging ±20 ms intervals from latency. 2.4. Event-related spectral perturbation and phase locking value

2. Methods 2.1. Subjects and stimulus presentation Fifteen right-handed university students (13 males, mean age: 23.5 ± 1.6 years) with no history of neurological or psychiatric illness participated in this study. All participants provided written informed consent before the experiment. Subjects performed an auditory novelty oddball task that was based on the random sequence of three types of stimuli consisting of a target (1000 Hz pure tone, p = 0.12, n = 48), novel (familiar environmental sounds, such as dog bark, buzz, and car crashing sound, p = 0.12, n = 48),

Trial-by-trial time–frequency decomposition was applied in the frequency range of 3.9–7.8 Hz (0.4 Hz steps) using continuous wavelet transforms implementing Morlet wavelets of five-cycle lengths. ERSP was then computed as follows:

ERSPð f ; tÞ ¼

N 1X jF n ðf ; tÞj2 ; N n¼1

where N is the total number of trials, F represents the complex numbers obtained by the wavelet transform, and f and t are discrete frequency and time instant values, respectively. ERSP values were normalized by the baseline average (400 ms preceding the stimulus

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onset). The PLV was calculated for each frequency f and time t point over N trials as follows (Lachaux, Rodriguez, Martinerie, & Varela, 1999):

   N 1 X  PLVð f ; tÞ ¼  expðjðu1 ðf ; t; nÞ  u2 ðf ; t; nÞÞÞ:  N  n¼1 Here, u designates the phase of signal that is computed by the arctangent of the imaginary part divided by the real part of the complex number F. As a result, PLV represents the consistency of the phase difference between two electrodes through repeated trials. The PLV was normalized by subtracting the baseline average and dividing by the baseline standard deviation (Rodriguez et al., 1999). In order to study the effect of selective processing of novel and target stimuli, differences were calculated by subtracting the standard from the novelty and target for each ERSP and PLV. The frequency band (4–6 Hz) and time window (200–600 ms) were determined by visually inspecting the global power of the time–frequency ERSP obtained by averaging all electrodes. All discrete frequency bins were averaged within the frequency band, and then latency was individually defined from the largest positive peak within the time window. The spectral powers within an interval of ±25 ms from the individual latency were averaged. The frequency bins and time points of the PLV were averaged by applying identical frequency bands and latencies with the ERSP. These ERSP and PLV from all electrodes or pairs were subject to non-parametric statistical tests (see below). 2.5. Statistical analysis The amplitude and latency of novelty P3 and target P3 were analyzed independently using a repeated measures analysis of variance (ANOVA). The within-subject variables were stimulus (2 levels: novel and target) and location (3 levels: Fz, Cz, and Pz). The Greenhouse-Geisser correction was used to evaluate F ratios to control for Type I errors in the repeated measure design. The Bonferroni correction for multiple comparisons was used in post hoc analyses. The significance level of all statistical tests was set to 0.05. ERSP was statistically compared between the novel and target stimuli and with each baseline period using a non-parametric permutation test (Maris & Oostenveld, 2007). To control for Type I errors in multiple comparisons, paired-sample statistical values were located under the permutation distribution. The permutation distribution was generated using statistical values that were obtained from the formula for the paired-samples of two subsets drawn by randomly permuting the two stimuli and all electrodes. Permutation p values were calculated using a Monte Carlo estimate, which was based on 5000 random permutations. The corresponding alpha levels were set to 0.05 of a two-tailed probability analysis.

To determine whether the PLV indicated significant neural synchrony between two specific electrodes during comparisons of both stimuli, we used a surrogate distribution obtained by calculating PLV from randomly shuffled trials (Lachaux et al., 1999). A total of 400 surrogate data points were calculated at each frequency and time segment and then normalized with respect to the baseline, similar to the normal PLV. The surrogate distribution was generated from statistical values for two subsets, which were randomly drawn. The p values were estimated using the proportion of statistical values of novel stimuli minus the target PLV from the surrogate distribution (Doesburg, Emberson, Rahi, Cameron, & Ward, 2008). The corresponding alpha levels were set to 0.05 of a one-tailed probability analysis. 3. Results 3.1. Averaged ERP component analysis Reaction time and accuracy for target stimuli were 611.9 ± 76.8 ms and 96.1%, respectively. Grand average ERP waveforms at three midline electrodes and the topographical distribution are shown in Fig. 1. The novelty P3 and target P3 were identified at about 300 ms at Fz and 400 ms at Pz from the stimulus onset, respectively. There was a significant main effect of stimulus for the novelty P3 amplitude (F1.0, 14.0 = 42.021, p < 0.001). However, there was no main effect of location (F1.4, 19.5 = 0.766, p = 0.41). The interaction between stimulus and location was significant (F1.8, 25.2 = 13.587, p < 0.001). Post-hoc analysis showed that the amplitudes of the novelty P3 were significantly higher in frontocentral regions than the target P3 (p < 0.001 at Fz and Cz). P3 amplitudes for target condition were obtained based on the latency derived at Pz for the Target condition for both novel and target conditions. There was a significant main effect for stimulus (F1.0, 14.0 = 9.241, p = 0.01) and location (F1.2, 16.5 = 37.285, p < 0.001). However, the interaction between stimulus and location was not significant (F1.5, 21.6 = 28.378, p = 0.202). Post-hoc analysis showed that the amplitudes of the target P3 were significantly higher than those of the novelty P3 (p = 0.001) in all electrode sites. Latency showed a significant main effect for stimulus (F1.0, 14.0 = 10.0, p = 0.007) and location (F1.5, 21.3 = 7.8, p = 0.005). However, the significance of the interaction between stimulus and location was not reached (F2.0, 27.9 = 0.9, p = 0.42). Post-hoc analysis revealed a significantly shorter latency for the novelty P3 in all 3 midline electrodes (p < 0.001 at Fz, Cz, and Pz). 3.2. Event-related spectral perturbation Fig. 2 shows time–frequency activation of the global power corresponding to the novel and target stimuli, which was obtained by averaging ERSP across all subjects and electrodes. Prominent

Fig. 1. (a) Grand averaged ERP waveforms at three midline electrodes for standard (black), target (blue), and novel (red) stimuli. (b) Voltage topographic scalp maps of novel and target P3s (left and right). (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)

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Fig. 2. Time–frequency activation patterns of standard (left), target (middle), and novel (right) ERSP, obtained by averaging all subjects and electrodes. The color bar represents the values of decibel power. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)

increases in the theta band (4–6 Hz) were observed at about 200– 600 ms for both novel and target stimuli. Theta activity showed a significantly higher power and earlier latency for the novel versus target stimuli (paired t-test, Power: novel = 3.09 ± 2.18, target = 2.13 ± 1.66, t = 2.28, p < 0.05; Latency: novel = 333.7 ± 80.5 ms, target = 390.3 ± 72 ms, t = 4.56, p < 0.001). The statistical topographic distribution using nonparametric permutation tests is presented in Fig. 3. A significant increase in theta activity was observed in the right frontal, central, parietal, and occipital electrodes for novel stimuli (left panel) and in the frontal, central and occipital electrodes for target stimuli (middle panel) compared to baseline (p < 0.0005, two-tailed). The contrast between novelty versus target (right panel) showed a significant increase in theta activity in right frontocentral regions (p < 0.05, two-tailed). However, the target stimuli did not result in significantly more activation compared to the novel stimuli.

Fig. 3. Topographic map of the theta bands (4–6 Hz) ERSP for novel versus baseline (left), target versus baseline (middle), and novel versus target stimuli (right). Black stars indicate significant electrodes (novel or target stimulus versus baseline: alpha < 0.0005, novelty versus target: alpha < 0.05). The time below each map denotes the mean latency and standard deviation obtained from individual peaks of theta power within a 200–600 ms time window.

Fig. 4. Topographic map of theta band phase synchrony for novel versus target (left) and target versus novel stimuli (right). Synchrony between electrode pairs is indicated by lines, which are drawn only if statistical values of the PLV were beyond the surrogate distribution of the randomly shuffled data set (alpha < 0.05). The color bar represents the number of synchronies at the electrode. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)

3.3. Phase locking value Fig. 4 depicts the statistical comparison of inter-regional phase synchrony of the theta band between novel and target stimuli. The color coding indicates the degree of summed synchrony in a given electrode. Considerable neural synchrony was observed for novel stimuli, primarily between the right frontal and left temporal regions in comparison to regions activated by target stimuli (left panel, p < 0.05, one-tailed). Target stimuli demonstrated significant neural synchrony between bilateral temporal and parietal regions compared to those activated by novel stimuli (right panel, p < 0.05, one-tailed).

4. Discussion In this study, we analyzed spectral power modulation and interregional phase synchrony of the theta band during an auditory novelty oddball task. As has been previously reported, task-irrelevant novel stimuli elicit a frontocentrally distributed novelty P3, and a task-relevant target stimulus elicits a parietal dominant target P3 (Friedman et al., 2001). In the present study, both novel and target stimuli elicited theta activities in the range of 200 to 600 ms after stimulation. Although considerable overlap was observed between novel and target response in spatial distribution, the non-parametric permutation test revealed that theta oscillation in the right frontal region was significantly related to novelty processing. Additionally, the inter-regional phase synchrony analysis revealed that the right frontal region was functionally connected to left temporal regions by oscillatory synchronization of theta activity. Overall theta power was higher for novel stimuli compared to target stimuli in the present study. The difference in theta power between novel and target stimuli was most significant at 300– 400 ms after stimulation in the right frontal region. This is in agreement with a previous study in which theta activity is more related to novel rather than target stimuli in a visual three-stimulus oddball task (Demiralp et al., 2001). It is also demonstrated that right frontotemporal areas are more significantly activated by novel stimuli. Additionally, novelty detection was affected in healthy aging and cognitive impairment, in which theta activity was significantly reduced (Cummins, Broughton, & Finnigan, 2008; Cummins & Finnigan, 2007). Patients with attention deficit hyperactivity disorder are known to show increased theta activity, which may be due to an increased effort in encoding of new information (Fallahpour et al., 2010). These findings suggest that theta oscillation may be related to processing novel stimuli. A PET study has suggested that right frontal cortical activation may be associated with the retrieval mode operation, which means an attempt to retrieve memory rather than be related to the actual access and retrieval of a stored memory trace (Klimesch et al.,

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2001; Tulving et al., 1996). ERP and fMRI studies have demonstrated that novelty processing may lead to fast access and retrieval of related semantic concepts, which engages the right prefrontal cortex (Mecklinger et al., 1997; Opitz et al., 1999). Moreover, an increase in right frontal theta activity has been observed during recognition, irrespective of retrieval success (Guderian & Duzel, 2005; Klimesch et al., 2001). Therefore, increased theta oscillation in the right frontal region in our study may indicate that the retrieval mode may have been engaged at a subconscious level in addition to an involuntary shift of attention during novelty processing. Significantly increased phase synchrony of the theta band between the right frontal and left temporal regions was observed in relation to the novelty P3 component in our study. However, the target P3 showed no significant connection between these two regions. This suggests that theta phase synchrony between the right frontal and left temporal regions may be specific to stimulus novelty, which is thought to reflect the functional communication of those cortical regions. Delta activity represents cognitive efforts that involve stimulus-matching and decisions with respect to the response to be made (Karakas, Erzengin, & Basar, 2000), hence the target P3 component. Because we considered only theta oscillation in our study, and the target P3 response is not at the theta frequency, the frontotemporal relationship observed in novelty P3 might not be present in the target condition due to the lack of a P3a response. A growing body of evidence suggests that left temporal regions play a critical role in semantic processing of objects (Martin, 1999). Furthermore, left temporal theta activity has been also implicated in the neural network for retrieving or, specifically, for a lexical– semantic retrieval (Bastiaansen et al., 2005; Guderian & Duzel, 2005). In this regard, our finding indicates that right frontal and left temporal regions may share a common neural mechanism related to memory retrieval during novelty processing. Thus, we hypothesize that theta phase synchronization between right frontal and left temporal regions may reflect the retrieval of memory traces for unexpected but familiar sounds from long term memory. However, it is well known that theta oscillation is related to process of working memory or encoding of incoming information. Furthermore, theta synchronization across distant brain regions might be characteristic of ‘top-down’ processes that use higher-level expectations and strategies to coordinate lower level perceptual and encoding processes (Kahana, Seelig, & Madsen, 2001). Collectively, our study supports the notion that novelty processing may be involved in automatic memory retrieval in the process of working memory and encoding process of incoming stimuli, in addition to attention switching to novel stimuli. fMRI studies have revealed two differential attentional networks: the dorsal and ventral frontoparietal networks (Corbetta, Patel, & Shulman, 2008). The dorsal attentional network is preactivated by the preparation of a specific response, linking relevant stimuli to responses, as in responding to target stimuli in our study. The ventral network detects salient stimuli and is not activated by task preparation. It has been reported that both the dorsal and ventral networks are activated simultaneously during reorienting when the stimuli appear at unattended locations, as for the novel stimuli in our experiment. Neural substrates of the ventral network include mainly the right temporo-parietal junction, the inferior and middle frontal gyrus, and the anterior cingulate. Based on this theory, the right frontal theta oscillation may be associated with activation of the ventral attentional network elicited by novel stimuli. There is a limitation to consider in the present study. Because the EEG signals measured on the scalp surface do not directly indicate the location of the active neurons in the brain, the precise spatial location in the brain should be confirmed by a high-

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