Elsevier

Brain Research

Volume 1362, 29 November 2010, Pages 56-67
Brain Research

Research Report
The effects of acupuncture on the brain networks for emotion and cognition: An observation of gender differences

https://doi.org/10.1016/j.brainres.2010.09.040Get rights and content

Abstract

Acupuncture modulates brain activity at the limbic–paralimbic–neocortical network (LPNN) and the default mode network (DMN). Since these brain networks show gender differences when mediating emotional and cognitive tasks, we thus hypothesize that women and men may also respond differently to acupuncture procedure at these brain regions. In order to test this hypothesis, we retrieved the data of 38 subjects, 19 females and 19 males, who had brain fMRI during acupuncture from previous studies and reanalyzed them based on sex status. Deactivation at the LPNN/DMN during needle manipulation of acupuncture was more extensive in females than in males, particularly in the posterior cingulate (BA31), precuneus (BA7m) and angular gyrus (BA39). The functional correlations between the right BA31 and pregenual cingulate (BA32), hippocampus or contralateral BA31 were significantly stronger in females than in males. The angular gyrus (BA39) was functionally correlated with BA31 in females; in contrast, it was anticorrelated with BA31 in males. Soreness, a major component of the psychophysical responses to needle manipulation, deqi, was correlated in intensity with deactivation of the angular gyrus in females; no such relationships were observed in males. In contrast to lesser deactivation at the LPNN/DMN networks, needle manipulation during acupuncture induced greater activation at the secondary somatosensory cortex and stronger functional connectivity with the anterior-middle cingulate (BA32/24) in males than in females. Our study suggests that brains with sex dimorphism may process the acupuncture stimulation differently between women and men.

Research Highlights

►Acupuncture modulates brain activity at the limbic–paralimbic–neocortical network (LPNN) and the default mode network (DMN). ►Deactivation at the LPNN/DMN during needle manipulation of acupuncture was more extensive in females than in males. ►However, needle manipulation during acupuncture induced greater activation at the secondary somatosensory cortex in males than in females. ►Soreness during acupuncture was correlated in intensity with deactivation of the angular gyrus in females; no such relationships were observed in males. ►Our study suggests that brains with sex dimorphism may process the acupuncture stimulation differently between women and men.

Introduction

Acupuncture, an ancient Chinese needle treatment, is used to relieve the clinical symptoms of pain, mood, and autonomic related disorders (Lundeberg et al., 2007). During the acupuncture procedure, needle is inserted at acupoints and then rotated manually. This manipulation of the needle after insertion induces deqi, a composite of unique sensations such as soreness, aching, pressure and heaviness, which is essential to the efficacy of acupuncture according to traditional Chinese medicine (Kong et al., 2007). It is proposed that pronounced action on the limbic system of the brain during the needle manipulation may underlie the beneficial effects of acupuncture on the clinical symptoms (Hui et al., 2007).

Using functional magnetic resonance imaging (fMRI), we and others have demonstrated that acupuncture produces deactivation of the limbic–paralimbic–neocortical network (LPNN) including the amygdala, hippocampus, septal nuclei, cingulate gyrus, precuneus and angular gyrus coupled with activation of the sensorimotor network (SMN) and a few paralimbic structures (Hui et al., 2005; Kong et al., 2007; Bai et al., 2007; Wang et al., 2007; Dhond et al., 2008, Fang et al., 2008; Qin et al., 2008). These limbic and limbic-associated structures have been shown to play a primary role in regulating emotion (Joseph, 1992; LeDoux, 1998). Furthermore, we have observed a marked similarity of the hemodynamic response to acupuncture with that of the default mode network (DMN) to attention tasks such as the cognitive examination (Buckner and Vincent, 2007; Raichle et al., 2001). The DMN structures modulated by acupuncture include 1) the frontal pole (FP) and the anterior cingulate in the medial prefrontal cortex (mPFC); 2) the hippocampus in the medial temporal lobe (MTL) and 3) the posterior cingulate (BA31), retrosplenial cortex (RSC) and precuneus (PCN) in the medial parietal cortex (MPC) (Bai et al., 2007, Dhond et al., 2008, Fang et al., 2008; Hui et al., 2005; Qin et al., 2008; Wang et al., 2007).

While sex is a biological term used to describe female vs. male, gender is a social term used to describe the identification of female vs. male. Although the majority of the studies do not measure sex hormones, except in some unusual situations, gender and sex are identical for the human subjects in the research studies. Studies have shown that the LPNN and DMN are sexually differentiated (Joseph, 2000), and sex dimorphisms exhibit significantly at the amygdala, hippocampus and neocortex (Juraska, 1991; Cahill, 2006). Functionally, gender differences in the brain are observed in the limbic system or the DMN when conducting emotional or cognitive tasks (Gur et al., 2000, Cahill et al., 2004, Goldstein et al., 2005). Though women seek complementary treatment modalities including acupuncture more frequently than men (Ben-Arye et al., 2009), the majority of studies evaluating acupuncture effects combine genders. Lund and Lundeberg (2008) have noticed that pain shows gender variations that might influence acupuncture treatment (Lund and Lundeberg, 2008)";. Brain fMRI shows the gender differences when experiencing calibrated pain (Kong et al., 2010a, Kong et al., 2010b) or during resting state (Kong et al., 2010a, Kong et al., 2010b). Because gender differences are shown in the LPNN and the DMN to mediate the tasks of emotion, cognition and pain and that these neural networks are also affected by acupuncture, we hypothesize that women and men may have different brain activation/deactivation patterns at the LPNN and the DMN in response to acupuncture procedure. In this study, using fMRI, we compared neural responses of the task-negative LPNN/DMN as well as the task-positive SMN in response to needle manipulation of acupuncture between two genders.

Section snippets

Subjects

Data on 38 subjects (19 females and 19 males) who had brain fMRI during acupuncture at matched acupoints were used for this study. All the subjects reported deqi sensations with a minimum total score of 3, and none reported sharp pain during needle manipulation. Females were comparable with males in age (Mean ± SE: 28.7 ± 1.8 vs. 29.4 ± 2.0) and ethnicity (percentage of Caucasian: 68% vs. 74%) (Table 1). There was no statistical difference in the total score of deqi between two genders (Table 1). The

Discussion

Female and male brains are similar in many aspects but different in others, which could lead to similar but also sex different neural responses depending on environmental stimuli (Witelson, 1991; Cahill, 2006). Pain shows gender variations that might influence acupuncture treatment (Lund and Lundeberg, 2008). This study revealed gender differences in the level of response and the preferential spatial distribution in each task-negative or task-positive network during needle manipulation of

Conclusion

To the best of our knowledge, this is the first report on the sex differences of the brain responding to the acupuncture stimulation as shown by fMRI. Significant gender differences were observed at both the LPNN/DMN networks and the sensation network in the brain. Since the modulation of these brain structures with acupuncture may be involved when used to treat clinical symptoms, our study suggests that the efficacy or action of acupuncture treatment might be different between women and men.

Subjects

The data from 38 subjects participating in a previous study were used (Hui et al., 2007) for this study analysis based on gender status. The subjects were right handed, generally healthy and screened to exclude those with neurological, psychiatric and medical disorders, and contraindications for exposure to high magnetic field. Experiments were conducted with the written consent of each subject and approved by the Massachusetts General Hospital Institutional Review Board.

Acupuncture

A single licensed

Acknowledgments

The manuscript is dedicated to Dr. Kathleen Kin-Sang Hui, who made a seminal contribution to link the acupuncture treatment with the modulation of brain function. We are saddened that she passed away while this manuscript was under review and consideration. This work was supported in part by a grant from the NIA, K23AG-022476 for W.Q.Q, and grants from the NIH/National Center for Complementary and Alternative Medicine (R21AT00978) (1-P01-002048-01) for K.K.H, (K01 AT003883) and (R21AT004497)

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