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Translational Neuroscience

Research Article • DOI: 10.2478/s13380-014-0208-8 • Translational Neuroscience • 5(1) • 2014 • 72-77

* E-mail: wangmufan@msn.com

Introduction

Love is a fundamental human experience which involves commitment, intimacy and passion between lovers [1-3]. Normal love creates strong family and social bonds, but pathological love, repetitive and uncontrolled attention and care towards one’s partner [4] in erotomania, obsessive-compulsive disorder, bipolar disorder or schizophrenia, brings burden to patients’ families and to society [5]. Under such circumstances, the patients often use automatic thinking in response to environmental stimuli and excessively seek out love-related information [4,6].

Studies have shown that love is involved in attention-related processing, such as reward, emotion, cognition, orientation or goal-directed motivation, which is based on its cerebral chemical correlates [7-12]. Using one of the neuroimaging techniques, the functional magnetic resonance imaging (fMRI), investigators found that some cortical and subcortical regions were related to the attentive processing of love, including the left inferior frontal gyrus, left middle temporal gyrus, mid insula, anterior cingulate cortex,

head of the caudate nucleus, ventral tegmental area, and cerebellum [10,13-18].

Compared to fMRI, the cerebral event-related potentials (ERP) have a higher time resolution to re�ect neural activities that happen within a second [19]. Using ERP techniques, Langeslag et al. [20] and Vico et al. [21] found larger activities, i.e. P3 and late positive potential components, at the time window from 350-700 ms in response to the faces of their lovers. This indicates increased attention, accompanied with strong positive affect or emotional arousal. Unfortunately, they found no “love effect” on the early ERP components such as N1, P2, or N2, implying that love only facilitates higher cognitive processing at a relatively later stage. However, as complex visual stimuli (faces) were adopted in the two studies, love-related information might only be obtained in a late stage, rather than an early or automatic stage. Considering a subliminal exposure (26  ms in duration) of love-related information was enough to elicit an e�ect in a very short time window (about 200 ms) [11,22], we assume that love’s facilitating e�ect also occurs via its in�uence on an early automatic cerebral processing or the involuntary attention.

Speech is one kind of stimulus which humans can rapidly process. Investigators have shown that early processing of speech is automatic and does not require participants to actively focus their attention on incoming speech [23,24]. The auditory mismatch negativity (MMN), one kind of classical cerebral ERP indicating the automatic response to any acoustic change [25], occurs in the time window of early auditory or semantic processing. MMN to spoken words reflects the automatic or semi-automatic speech-sound traces [24,26,27], or indicates an initial access to semantic information related to spoken words [24,28]. Thereafter, MMN elicited by spoken words would be a wonderful candidate to reflect an early processing of love-related information within speech.

On the other hand, according to the best of our knowledge, there have been no studies addressing the early cognition of love oriented to a participant by their lover yet. As love is a goal-direct state towards an individual’s beloved [7-9], perception and expression of love from the beloved would be sought after by their lover. In such a case, love related information expressed by an individual’s own lover might be detected earlier in that individual. In our current study,

1Department of Clinical Psychology and Psychiatry / School of Public Health,

Zhejiang University College of Medicine, Hangzhou, China

2Key Laboratory of Medical Neurobiology of Chinese Ministry of Health and of Zhejiang

Province, Hangzhou, China

Hao Chai1,2, Wanzhen Chen1,2,

You Xu1,2, Jing Hu1,2,

Shaofang Xu1,2,Jinhua Zhang1,2,

Wei Wang1,2*

Received 23 October 2013 accepted 05 March 2014

MISMATCH NEGATIVITY TELLS YOU HOW MUCH YOU AUTOMATICALLY CARE FOR YOUR LOVER’S LOVEAbstractUnderstanding the automatic process of love oriented to a participant by his or her own lover helps to build a normal loving relationship. It also helps to elucidate some of the underlying mechanisms of pathological love, which involves both repetitive and uncontrolled attention and care. Previous studies have addressed the late-stage process of love, but its early or automatic stage has been studied less. When processing a change in speech from “love” to “love you” from their own lover, participants showed a more prefrontal-frontal distribution of cerebral mismatch negativity. Source analysis showed that the left superior temporal gyrus was involved in all participants. The right inferior frontal gyrus was additionally involved in some participants who evaluated love as more intense. Brain areas activated in process might inversely indicate how much a participant cares about the love oriented by their lover.

Keywords • Heterosexual love • Left superior temporal gyrus • Mismatch negativity • Right inferior frontal gyrus • Standardized Low Resolution Electromagnetic Tomography (sLORETA)

© Versita Sp. z o.o.

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we asked participant’s lovers to pronounce “爱

(ai)” (love) and “爱你 (ai ni)” (love you). Later we tested our participants using these words: the standard stimulus, “ai”, was composed of love information but without orientation, while the deviant stimulus, “ai ni”, was composed of love information that was clearly oriented to the participant. The subtraction of the brain waves (i.e., MMN) to these stimuli would reflect the recognized love orientation by the participant. Moreover, we evaluated the love intensity between a participant and their lover using a questionnaire, in order to control the variances of the cerebral response. We hypothesized that scalp topographic features of MMN to the spoken words would vary according to di�erent intensities of love, and the MMN generators would clearly tell us the brain areas responsible for the orientation of love.

Experimental Procedures

ParticipantsTwenty-seven participants (12 women and 15 men, mean age: 21.3 years ± 2.1 SD) were university students who were involved in heterosexual relationships. The mean duration of their relationship was 15.4 months with 10.0 S.D (range: 6 - 42 months). All participants had no history of psychiatric or neurological abnormalities and had to refrain from drug and alcohol use for at least 72 hours prior to the test. The study was approved by a local ethics committee, and written informed consents were obtained from all participants after the nature and possible consequences of the study enrollment were explained.

ProcedureAll participants received a short inventory, the Love Intensity Scale (LIS), which assessed the feelings they had about the love between themselves and their lovers. The LIS contains eight items which are derived from the triangle theory of love [1]: (1) I think my lover is excellent; (2) We can understand each other; (3) I would like to share my feelings with my lover; (4) I would like to share my properties with my lover; (5) I could receive support from my lover; (6) I could support my lover; (7) My lover and I could communicate intimately; and (8) I think

we fit perfectly with each other. The inventory is scored with a sum of the answers to the eighth items with the Likert ratings (1 - very unlike me, 2 - moderately unlike me, 3 - somewhat like and unlike me, 4 - moderately like me, 5 - very like me). A higher LIS score indicates a more intense love. The mean LIS score of all participants was 35.9 ± 4.3 SD, and the internal reliability (the Cronbach’s α) was 0.88 in the present study. Based on the mean LIS score, the participants were divided into two groups for further analysis: the higher (Higher group, LIS > 36, n = 15, 6 women and 9 men) and the lower (Lower group, LIS ≤ 36, n = 12, 6 women and 6 men) love intensity group. Afterwards, participants of both groups underwent ERP testing.

Stimuli and ERP designParticipants were seated in an armchair in a quiet room and speech stimuli were delivered through headphones at an inter-stimulus interval 0.625 s (1.6 Hz). The standard (frequent) stimulus was “爱 (ai)” (love) and the deviant (rare) stimulus was “爱你 (ai ni)” (love you). Both stimuli were pronounced by the lovers of each participant. The duration of the standard stimulus was fixed at 270 ms and the duration of the deviant stimulus was 330 ms. The standard stimuli were delivered 450 times (90%) while the deviant ones were delivered 50 times (10%) in a randomized order. Each participant was aware that the incoming speech stimuli would be pronounced by their own lover. With a pen in their dominant hand, subjects were instructed to arrange series of seven randomized digits (selected from 0 to 9) to draw their attention away from the incoming stimuli.

ERP recordingThe electroencephalography (EEG) recordings were performed with 32 electrodes embedded in an electro-cap (Electro-Cap International, Inc), according to the 10-20 International System and intermediate positions (Fp1, Fpz, Fp2, F3, F4, F7, F8, Fz, Fc1, Fc2, Fc5, Fc6, T7, T8, C3, C4, Cz, Cp1, Cp2, Cp5, Cp6, P3, P4, P7, P8, Pz, O1, Oz, O2, POz, M1, M2). Recordings were made with an average reference and then referred again off-line to the average activity of the two mastoid electrodes (M1 and M2). The EEG was amplified by an ANT amplifier (ANT B.V., Enschede, The Netherlands)

and the impedance of all electrodes was kept below 5 kΩ. The EEG was continuously recorded with a sampling rate of 512 Hz. Trials containing electrooculogram (EOG) and other artifacts were eliminated off-line by ASA software (ANT software, version 4.7., ANT Software B.V., Enschede, The Netherlands). Data were filtered with a bandpass of 0.1 - 30  Hz. The sampling epoch was 100 ms pre-stimulus and 500 ms post-stimulus. A sweep in which the EEG exceeded ± 70 μV was excluded from averaging.

MMN was obtained by subtracting the ERP elicited by standard stimuli from those elicited by deviant stimuli. MMN waves were analyzed by their peak latency and baseline-to-peak amplitude of the most negative de�ection in the time windows of 100 - 250 ms.

Statistical analysesA four-way ANOVA, Group (2) x Gender (2) x Sagittal positions (3: prefrontal, frontal, and central) x Lateral positions (3: left, central, and right) with post-hoc Bonferroni test, was performed on nine selected electrodes (Fp1, Fpz, Fp2, F3, Fz, F4, C3, Cz, C4) according to the frontal-central scalp distribution of the MMN [25]. The α level of significance (p) was set at 0.05. With the present sample size, power to detect an effect (such as an MMN amplitude on one electrode) was greater than 80% at p < 0.05 in a sample of 12 subjects per group (the smaller group in the present study).

Source localization analysis for the MNN were performed in both groups computed by standardized Low Resolution Electromagnetic Tomography (sLORETA) [29] using ASA software (ANT Software B.V., Enschede, The Netherlands). The solution spaces of sLORETA were calculated on a standard head model from the Montreal Neurological Institute [30]. Based on the sLORETA results, a source level statistical analysis was performed by statistical parametric mapping (SPM 8, http://www.fil.ion.ucl.ac.uk/spm) toolbox on M/EEG data to detect any differences in MMN sources between groups.

Results

Each participant showed clear ERP traces to standard and deviant stimuli at all 32 electrodes.

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The MMN grand averages at nine electrodes are shown in Figure 1. No gender (F1,23 = 0.82, MSE = 2801.28, p = 0.38) or group effect (F1,23 = 0.96, MSE = 3302.95, p = 0.34) was detected for MMN latencies. MMN latencies did not differ between electrode positions either: sagittal effect (F2,46 = 0.35, MSE = 361.8, p = 0.59); lateral effect (F2,46 = 1.49, MSE = 222.28, p = 0.24 ).

Moreover, no significant gender effect (F1,23 = 1.30, MSE = 5.39, p = 0.27) was detected for MMN amplitudes. There was however, a significant group effect on the MMN amplitudes (F1,23 = 8.20, MSE = 34.11, p < 0.01), with larger amplitudes found in the Lower group (-1.96 μV ± 1.17; p = 0.01, 95% CI: 0.21 - 1.31) than in the Higher group (-1.19 μV ± 0.98). For electrode positions, lateral effect (F2,46 = 2.02, MSE = 0.63,p = 0.16) was not statistically significant. By contrast, sagittal effect (F2,46 = 14.06, MSE = 28.69, p < 0.001) was statistically significant and larger MMN amplitudes were found at prefrontal (-1.74 μV ± 1.26; p = 0.01, 95% CI: 0.21 - 1.50) and frontal (-1.90 μV ± 1.15; p < 0.01, 95% CI: 0.54 - 1.48) electrodes than those found at central electrodes (-0.95 μV ± 0.63). Interaction of group X sagittal electrode position (F2,46 = 5.24, MSE = 10.68, p <0.05) was significant. Post-hoc test showed that MMN

amplitudes were larger at prefrontal and frontal electrodes than those at central electrodes (all p values < 0.001) in the Lower group, compared to the Higher group.

Following the significant group and group X electrode interaction effects on MMN amplitude, we tried to locate the possible neural sources for MMN in two groups by performing the sLORETA in the 150-250 ms time windows separately in the two groups. Group differences regarding the MMN sources are illustrated in Figure 2. Specifically, the inverse solution showed that the processing of the love orientation was associated with two putative generators in the right frontal lobe (BA 45, the right inferior frontal gyrus) and the left temporal lobe (BA 22, the left superior temporal gyrus) in the Higher group, but only with one putative generator in the left temporal lobe (BA 22, the left superior temporal gyrus) in the Lower group (Table 1). Moreover, the source level statistical analysis showed signi�cantly less activity at the left superior temporal gyrus (t = 1.91, p = 0.03), as well as signi�cantly more activity at the right inferior frontal gyrus (t = 2.03, p = 0.03) in the Higher group, compared to those in the Lower group.

Discussion

After dividing our participants into the higher and lower love intensity groups, we found a more prefrontal-frontal distributed MMN amplitude, especially in the Lower group. The left superior temporal gyrus was involved in both Higher and Lower groups, and its activation was signi�cantly higher in the latter group. An additional generator, the right inferior frontal gyrus, was more involved in the Higher group than it was in the Lower group. To the best of our knowledge, this is the �rst study that has demonstrated that two putative brain areas are responsible for the automatic processing of love orientation recognized by the participant.

Topographically, smaller MMNs at the prefrontal and frontal electrodes were detected in the Higher group, compared to those detected in the Lower group. This might be due to the contributions of the right inferior frontal gyrus in generating MMNs in the Higher group. The dominance of the left superior hemisphere per se was counteracted by the right inferior brain activation in those participants.

Earlier linguistic studies [27,28,31,32] showed that the temporal areas are involved

Figure 1. Grand averages of mismatch negativity (MMN) and electrooculogram (EOG) in participants reporting higher (dotted lines, n = 15) and lower (solid lines, n = 12) love intensities between them and their own lovers.

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in generation of MMN to words, and the contribution is always left-dominant. Moreover, the source located in the left superior temporal area was thought to reflect the early access to semantic context of spoken words [33,34]. Thus, in line with

past research, the present activations also indicate an early detection of the semantic information (i.e. love orientation recognized by the participant).

Interestingly, when the love intensities evaluated by our participants were higher,

an additional brain area, the right inferior frontal gyrus, was activated. Recent studies have shown that this area is indeed recruited when unexpected important cues are detected [35,36]. The findings are also in accordance with past studies which have

Table 1. Magnitude, Talairach (T) coordinates, and putative mismatch negativity (MMN) generators according to the active source analyses by sLORETA in the 150-250 ms time window in participants reporting higher (Higher, n = 15) and lower (Lower, n = 12) love intensities between them and their own lovers.

Magnitude (nA)T-coordinates (mm)

Lobe (Gyrus, BA)X Y Z

Higher 2.21 58.4 19.2 14.8 Right frontal lobe (inferior frontal gyrus, BA 45)

1.54 -47.7 -14.3 1.4 Left temporal lobe (superior temporal gyrus, BA 22)

Lower 2.43 -47.8 -13.4 -8.2 Left temporal lobe (superior temporal gyrus, BA 22)

Figure 2. Active source analysis by standardized Low Resolution Electromagnetic Tomography (sLORETA) in the 150-250 ms time window of mismatch negativity (MMN) to love-related spoken words in participants reporting higher (A, n = 15) and lower (B, n = 12) love intensities between themselves and their lovers.

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457, 148[18] de Boer A., van Buel E.M., Ter Horst G.J., Love is more than a kiss: a

neurobiological perspective on love and a�ection, Neuroscience, 2012, 201, 114-124

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found that the obsessive behavior found in early-stage lovers is similar to that found in obsessive-compulsive disorder patients [16,37]. Neuroimaging studies conducted in obsessive-compulsive patients also exhibited changes in the right inferior frontal gyrus [38,39].

Several neurotransmitters, dopamine and 5-HT, affect MMN morphology [40]. A blockade of dopamine D2 receptors increases MMN to an involuntary detection of task-irrelevant stimuli [41]. In addition, the underlying mechanism of obsessive behavior is suggested to be an increase in dopamine coupled with a decrease in serotonin [16]. Both dopamine and 5-HT were found in the fronto-temporal areas, including BA 45, especially when the love was intense [14,16-18].

Regarding the limitations of our study design, firstly, physically length-similar stimuli without love information were not used in the present study. Implementing such stimuli in a future study would clarify whether the observed effects in the current study are specific to the love domain. Secondly,

our participants were university students. Whether the love orientation automatically initiates similar brain area activities in normal people of other ages, or in patients with pathological love, remains to be seen. Finally, we did not use a standardized voice or other people’s voices as a control. Therefore, our results could not be generalized to other kinds of love, such as homosexual love or parental bonding.

In conclusion, we used the MMN to examine love-related spoken words in participants engaged in heterosexual love because of its superiority to other neuroimaging techniques in the detection of automatic brain processing. The automatic processing of the recognized love orientation activated the left superior temporal gyrus, and additionally activated the right inferior frontal gyrus when the love was more intense. Our study provides an option to assess how much a participant cares about their lover’s love involuntarily, and might help to depict brain mechanisms of a pathological love in future studies.

Acknowledgments

The study was supported by a grant from the National Natural Science Foundation of China (No. 91132715) to W. Wang.

All authors had full access to all the data in the study and take responsibility for the integrity of the data and the accuracy of the data analysis (Study concept and design: W.W. Acquisition of data: H.C., W.C., and S.X. Analysis and interpretation of data: H.C. and Y.X. Writing the draft of the manuscript: W.W. and H.C. Critical revision of the manuscript for important intellectual content: J.H. and J.Z.).

The authors are grateful to H. Qian and R. Li for collecting some data described in the report and to Dr. Judy Fleiter, Queensland University of Technology and Dr. Jared Stern, the 2nd affiliated hospital of Zhejiang University College of Medicine, for checking the English language used in this report.

The study was performed in accordance with the Declaration of Helsinki and the approval of the local ethical committee. The authors declare no conflict of interest.

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