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Effect of Bilingualism in the Anterior Cingulate Cortex: A Proton Magnetic Resonance Spectroscopy Study in Two Centres

Jubin Abutalebi1, Carrie Chiu2, Henry Mak2, Brendan Stuart Weekes2, 3* and Linda Zhang2
  • 1 University Vita-Salute San Raffaele, Italy
  • 2 University of Hong Kong, Hong Kong, SAR China
  • 3 University of Melbourne, Australia

The aim of this study was to determine whether 1H magnetic resonance spectroscopy (MRS), is correlated with years of bilingual experience and different to monolingual controls. Proton magnetic resonance spectroscopy (1H-MRS) uses MRI techonology to detect differences in neuroplasticity by measuring critical neurochemicals (neurotransmitters and metabolites). It is a noninvasive and repeatable measurement of in vivo brain chemistry. MRS has potential to provide insights into the neurobiology of bilingualism as well as mediators and moderators of language learning. For example, excitatory glutamatergic neurons are the most abundant cortical neurons in brain, taking up 60–80% of glucose oxidation and energy consumption. Glutamate is also a very abundant neurotransmitter (90% of synapses), playing an important role in neurodevelopmental processes such as neural growth, migration, differentiation, and neural plasticity (Baruth et al., 2013; Bejjani et al., 2012; Chiu et al., 2014; Page et al., 2006). Study aims and hypotheses To measure the levels of circulating glutamate that reflects excitatory activity in the anterior cingulate gyrus a region known to differentiate bilingual from monolingual speakers; and correlate circulating glutamate to performance on a test of executive function. The hypothesis is bilingual and monolingual speakers will have different levels of Glx which is a summation of glutamate (Glu) and glutamine (Gln). Method A group of 21 healthy young bilingual subjects (10 males; mean age ± standard deviation = 24.19 ± 2.25 years; age range 20-30 years; education = 17.6 ±1.55 years; range 15-20 years) was recruited among the university students in Hong Kong. All of them were bilingual speaking English and Cantonese. Participants with history of neurological and psychiatric illnesses were excluded. Subjects' Socio Economic Status (SES) was assessed using a self-rated questionnaire (mean = 45.18 ± 5.49; range: 31-54). A matched group of 20 healthy young monolingual subjects (11 males; mean age = 24.40 ± 2.11 years; age range 20-28 years; mean education = 16.80 ±1.61 years; range 15-20 years) was recruited among the university students in Milan. Again, participants with history of neurological and psychiatric illnesses were excluded. Written informed consent was obtained from all participants. The protocol of the study was approved by both the University Vita-Salute San Raffaele Research Ethics Committee and the Human Research Ethics Committee of the University of Hong Kong. Non-parametric Mann-Whitney test showed no significant difference for all matching criteria, e.g. age (p = 0.250), education (p = .119) between the bilingual and monolingual groups. MR scanning All MR scans on bilingual subjects were performed using a 3.0 T scanner (Achieva TX, Philips Healthcare, Best, The Netherlands). A sensitivity encoding (SENSE)-head-8- coil was used. A standardized axial T1W 3D volumetric fast field echo (FFE) sequence was employed with the following imaging parameters: repetition time TR/TE = 8.0/3.9 ms, voxel size = 1×1×1 mm3, field of view = 230×183 mm2, slices = 150, reconstruction matrix = 256, flip angle 8° and turbo field echo factor = 163. Images acquired from T1W 3D FFE were employed for the positioning of single voxel spectroscopy (SVS) for proton magnetic resonance spectroscopy (1H-MRS). Point resolved spectroscopy (PRESS) was used as the volume selection method for the region-of-interest and excitation was employed method for water suppression. Scanning parameters are TR/TE = 2000/39 ms, number of signals averaged = 128, phase cycles = 16, spectral width = 2000 Hz with spectral resolution of 1.95 Hz per point, and free induction decay = 1024. For shimming, pencil-beam-auto was employed. SVS of size 2×2×2 cm3 was placed in the dorsal ACC (Figure 1). The whole scan took approximately 20 min. Monolingual participants had MR scanning at the C.E.R.M.A.C (Centro di Eccellenza Risonanza Magnetica ad Alto Campo) at University San Raffaele in Milan, Italy. Same scanner model and exam cards (T1W 3D FFE and 1H-MRS) used to scan bilingual subjects in Hong Kong were employed to scan all monolingual subjects to enhance comparability of images. Results The 1H-MRS spectra were processed using QUEST (quantification based on quantum estimation) within jMRUI 4.0. Metabolites, i.e. choline (Cho), creatine (Cr), N-acetly aspartate (NAA), myo-inositol (mI), and Glx [summation of glutamate (Glu) and glutamine (Gln)], were measured and quantified as described in Chiu et al., 2014 (Figure 1). In order to account for the difference in water content in gray matter (GM), white matter (WM) and cerebrospinal fluid (CSF), voxel-based morphometry (VBM) was used to determine the GM, WM and CSF composition within the SVS, as detailed in our previous publications (Chiu et al., 2014; Mak et al., 2011). Furthermore, correction factors for T1 and T2 values were also implemented (Chiu et al., 2014). Mean levels of Glutamate + Glutamine were significantly lower for bilinguals (14.66±1.87) than monolinguals (15.13±1.42) p<0.045. Conclusions The action of neuromodulators regulates balance in neurotransmitters essentially disinhibiting the local circuitry to enable adult learning. Glutamate is a primary excitatory neurotransmitter. Molecular triggers to plasticity can shift neural circuits from an immature to an excited state, thus allowing learning. Neuromodulatory circuits that dampen cognitive processing (GABA) are molecular brakes and thus have lower levels of glutamate. The results suggest Glx may be lower in bilinguals because of greater inhibitory control over language usage on a daily basis (Abutalebi et al. 2013). Figure 1. (a) Position of voxel placed in the dorsal anterior cingulate cortex, (b) simulated spectrum using the parameter QUEST in jMRUI, (c) acquired spectrum (red) superimposed on the simulated spectrum (blue) from QUEST.

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References

Abutalebi, J., Della Rosa, P. A., Green, D. W., Hernandez, M., Scifo, P., Keim, R., Cappa, S. F. & Costa, A. (2012). Bilingualism tunes the anterior cingulate cortex for conflict monitoring. Cerebral Cortex, 22, 2076-86.

Baruth, J. M., Wall, C. A., Patterson, M. C., and Port, J. D. (2013). Proton magnetic resonance spectroscopy as a probe into the pathophysiology of autism spectrum disorders (ASD): a review. Autism Research, 6, 119–133. doi: 10.1002/aur.1273

Bejjani A, O'Neill J, Kim JA, Frew AJ, Yee VW, Ly R, et al. (2012) Elevated Glutamatergic Compounds in Pregenual Anterior Cingulate in Pediatric Autism Spectrum Disorder Demonstrated by 1H MRS and 1H MRSI. PLoS ONE 7(7): e38786. https://doi.org/10.1371/journal.pone.0038786

Chiu, P. W., Mak, H. K., Yau, K. K., Chan, Q., Chang, R. C. & Chu, L. W. (2014). Metabolic changes in the anterior and posterior cingulate cortices of the normal aging brain: proton magnetic resonance spectroscopy study at 3 T. Age (Dordr), 36, 251-64.

Mak, H. K., Zhang, Z., Yau, K. K., Zhang, L., Chan, Q. & Chu, L. W. (2011). Efficacy of voxel-based morphometry with DARTEL and standard registration as imaging biomarkers in Alzheimer's disease patients and cognitively normal older adults at 3.0 Tesla MR imaging. Journal of Alzheimers Disease, 23, 655-64.

Page, L.A., Daly, E., Schmitz, N., Simmons, A., Toal, F., et al. (2006) In vivo 1H-magnetic resonance spectroscopy study of amygdala-hippocampal and parietal regions in autism. Am J Psychiatry 163: 2189–2192.

Keywords: Choline (Cho), Creatine (Cr), N-acetly aspartate (NAA), Myo-inositol (mI), Glutamate

Conference: Academy of Aphasia 55th Annual Meeting , Baltimore, United States, 5 Nov - 7 Nov, 2017.

Presentation Type: poster or oral

Topic: General Submission

Citation: Abutalebi J, Chiu C, Mak H, Weekes B and Zhang L (2019). Effect of Bilingualism in the Anterior Cingulate Cortex: A Proton Magnetic Resonance Spectroscopy Study in Two Centres. Conference Abstract: Academy of Aphasia 55th Annual Meeting . doi: 10.3389/conf.fnhum.2017.223.00108

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Received: 02 May 2017; Published Online: 25 Jan 2019.

* Correspondence: Prof. Brendan Stuart Weekes, University of Hong Kong, Hong Kong, Hong Kong, SAR China, 481709@frontiersin.org