The relationship between bilingual experience and gyrification in adulthood: A cross-sectional surface-based morphometry study

Brain and Language 198 (2019) 104680

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The relationship between bilingual experience and gyrification in adulthood: A cross-sectional surface-based morphometry study Nicola Del Maschio, Davide Fedeli, Simone Sulpizio, Jubin Abutalebi

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Centre for Neurolinguistics and Psycholinguistics (CNPL), University Vita-Salute San Raffaele, Milano 20132, Italy

A R T I C LE I N FO

A B S T R A C T

Keywords: Cingulate cortex Entorhinal cortex Bilingualism Gyrification Neuroplasticity Surface-based morphometry

Neuroimaging evidence suggests that bilingualism may act as a source of neural plasticity. However, prior work has mostly focused on bilingualism-induced alterations in gray matter volume and white matter tract microstructure, with additional effects related to other neurostructural indices that might have remained undetected. The degree of cortical folding or gyrification is a morphometric parameter which provides information about changes on the brain’s surface during development, aging and disease. We used Surface-based Morphometry (SBM) to investigate the contribution of bilingual experience to gyrification from early adulthood to old age in a sample of bilinguals and monolingual controls. Despite widespread cortical folding reductions for all participants with increasing age, preserved gyrification exclusive to bilinguals was detected in the right cingulate and entorhinal cortices, regions vulnerable with normal and pathological brain aging. Our results provide novel insights on experience-related cortical reshaping and bilingualism-induced cortical plasticity in adulthood.

1. Introduction Neural plasticity, a general description of how the brain changes, relies on the property of neural circuits to be modified, structurally and functionally, by experience-evoked neural activity. The brain has been found to be plastic in numerous studies showing that structure can be modified depending on specific forms of individual expertise such as professional musicianship (e.g. Steele, Bailey, Zatorre, & Penhune, 2013; Wan & Schlaug, 2010), simultaneous interpreting (e.g. Elmer, Hänggi, & Jäncke, 2014) and long-term meditation practice (Luders et al., 2012). Gray and white matter responsiveness has also been associated with the acquisition and use of a second language (L2) (Coggins, Kennedy, & Armstrong, 2004; Osterhout et al., 2008), which entails not only the acquisition of additional linguistic knowledge, but also the skills necessary to select and control two languages according to the given communicative circumstances (see Pliatsikas, 2019a). A causal relationship between L2 learning and neurostructural changes has been demonstrated in young adults by longitudinal investigations with mid- or long-term L2 training components (e.g. Hosoda, Tanaka, Nariai, Honda, & Hanakawa, 2013; Mårtensson et al., 2012). Most recently, Legault, Grant, Fang, and Li (2019), used structural MRI to examine changes in cortical thickness (CT) and gray matter volume (GMV) across two semesters of L2 classroom learning. Participants

underwent MRI scanning and L2 testing at two time points ~4 months apart. At the second session of testing, second language learners showed increased CT as compared to controls in the left anterior cingulate cortex (ACC) and right middle temporal gyrus (MTG), with a positive association between CT in the right MTG and behavioral performance in a language decision task. CT increase in the left ACC also correlated with functional connectivity between ACC and MTG. These findings have been interpreted as indicating that L2 lexical development in young adults is associated with structural and functional modifications in regions important for lexico-semantic processing (i.e., MTG) and language control (i.e., ACC). Remarkably, recent observations indicate that neuroplastic changes may occur after only one hour of vocabulary training in L2 (Hofstetter, Friedmann, & Assaf, 2017) and vary based on L2 learning contexts (Legault, Fang, Lan, & Li, 2019). When cross-sectionally comparing bilingual and monolingual older adults, bilinguals showed higher brain integrity in regions and circuits underpinning bilingual language processing and suffering from early or greater-thanaverage degradation with increasing age. For instance, preserved integrity for bilingual versus monolingual older adults has been reported in a cingulo-fronto-parietal network associated with executive control1 (e.g. Del Maschio, Sulpizio, & Gallo et al., 2018; Luk, Bialystok, Craik, & Grady, 2011) and anterior temporal lobe structures implicated in semantic memory (Abutalebi et al., 2014; Olsen et al., 2015). Group

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Corresponding author at: Vita-Salute San Raffaele University, Via Olgettina, 58, 20132 Milan, Italy. E-mail address: [email protected] (J. Abutalebi). 1 “Executive control” or “executive functioning” may be characterized as a multi-componential construct comprising a set of general-purpose, top-down processes regulating goal-directed behavior (Miyake & Friedman, 2012). https://doi.org/10.1016/j.bandl.2019.104680 Received 29 March 2019; Received in revised form 13 August 2019; Accepted 14 August 2019 0093-934X/ © 2019 Elsevier Inc. All rights reserved.

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gyrification and years of meditative practice. It is noteworthy that the aforementioned studies are mostly concerned with environmentallyinduced plasticity at the cortical surface level and do not control for gyrification-cognition relationships. Emerging research on normal populations shows, however, that a higher degree of cortical folding may have positive repercussions on cognitive processing (e.g. Gautam, Anstey, Wen, Sachdev, & Cherbuin, 2015; Liu et al., 2012). The executive control performance of healthy adults, for instance, measured on mental flexibility and working memory tasks, has been positively correlated with frontal and parietal gyrification after controlling for cortical volume (CV), CT and SA (Gautam et al., 2015; Green et al., 2018). At present, the specific neurobiological basis for this functional advantage is incompletely understood. On the one hand, a larger cortical surface fitted into a limited cranial volume contains more neuropile and – in principle – a larger number of neurons, potentially providing greater computational power to the brain (but see Mota & Herculano-Houzel, 2015; Neves et al., 2018). On the other hand, cortex folding brings together interconnected cortical areas distantly positioned along the cortical mantle, thus favoring – in principle – high speed neural communication through minimized signaling costs in terms of distance traveled and time taken to propagate signals (Chklovskii, Schikorski, & Stevens, 2002; Klyachko & Stevens, 2003). The findings above mentioned raise the possibility that a cognitively stimulating experience such as bilingualism may impact gyrification in regions and circuits implicated in bilingual language processing and vulnerable to aging, resulting in preserved brain integrity and potentially maintained cognitive function. Compared to other structural metrics, gyrification appears to be differentially sensitive both to age and environmental factors (Jockwitz et al., 2017; Luders et al., 2012; Madan & Kensinger, 2018), thus supporting a direct investigation of this parameter in the context of bilingualism and aging research. The present study focuses on cingulo-fronto-parietal structures associated with executive control processes and temporal lobe regions implicated in memory functions. We used a proxy measure of cortical folding, that is cortical curvature, to establish the global and regional effects of bilingual experience on gyrification across the adult lifespan in a sample of bilingual and monolingual participants. A classic test of executive control – that is, the Flanker Task (Fan, Mccandliss, Fossella, Flombaum, & Posner, 2005) – was used to investigate putative bilingualism-related effects on gyrification-cognition mappings. Associations between local gyrification and L2 proficiency/age of acquisition were also inspected to provide additional clues on bilingualism-mediated cortical plasticity. Our main prediction is that older adult bilinguals will exhibit preserved cortical folding compared to monolingual controls in key cingulo-fronto-parietal and temporal lobe structures.

differences in the cingulo-fronto-parietal network have been attributed to the increased cognitive load for inhibition (i.e., the ability to suppress dominant responses), shifting (i.e., the ability to switch between tasks), and monitoring (i.e., the ability to update information in working memory) that the simultaneous management of multiple languages entails over the lifespan (Abutalebi & Green, 2016). Differences in anterior temporal structures have been posited to result from the greater cognitive and memory demands that the processing of a larger vocabulary place on bilingual learners (Abutalebi et al., 2014; see also Perani et al., 1998). Combined with the evidence that bilinguals stave off dementia symptoms for longer than monolingual controls (e.g. Alladi et al., 2013; Bialystok, Craik, & Freedman, 2007; Perani et al., 2017), the aforementioned findings have led to the interpretation that bilingualism may lead to a neural reserve in aging populations (see, for discussion, Del Maschio, Fedeli, & Abutalebi, 2018). Neural reserve has been defined, in other contexts, as the capacity for resilience to the expected age-related deterioration and pathology of the brain (Barulli & Stern, 2013). Practically, neural reserve has been mostly measured by GMV, CT and white matter (WM) integrity (Stern, 2017). These same parameters have been adopted in morphological studies investigating bilingualism as a source of plasticity and neuroprotection in aging (for review, see Pliatsikas, 2019b). Of note, prior work on bilingualism-associated changes in gray matter has generally employed Voxel-Based Morphometry (VBM) (Ashburner & Friston, 2000), which relies on a purely volumetric representation of the brain and uses image intensities to yield composite measures of GM volume or density. Compared to VBM, recent advances in cortical surface reconstruction offer supplemental and more specific information on brain structure and age-related morphometric changes (Lemaitre et al., 2012). Surface-Based Morphometry (SBM) methods, for instance, hinge upon an explicit reconstruction of the cortex geometry to investigate additional parameters of cortical anatomy such as (surface-based) CT, surface area (SA), cortical folding or gyrification, and sulcal depth. SBM may thus lead to further insight not only into the neuroanatomical correlates of bilingualism, but also into so far undetected components of neural reserve associated with bilingual experience. Furthermore, although preserved brain integrity is likely associated with cognitive maintenance in normal aging (see, Stern, 2017), an aging effect on bilinguals’ cognitive performance has been shown to be not necessarily mediated by aggregate indices such as GMV (Del Maschio, Sulpizio, & Gallo et al., 2018; Gold, Johnson, & Powell, 2013). It is plausible that additional cortical features may act as modulators of cognitive performance across adulthood in bilingual individuals. The aim of the present study is to investigate the contribution of bilingual experience to cortical folding or gyrification from early adulthood to old age in a sample of bilinguals and monolingual controls. Gyrification is a quantitative feature of cortex anatomy which provides valuable information about changes on the brain’s surface during development, aging and disease (e.g. Cao et al., 2017; White, Su, Schmidt, Kao, & Sapiro, 2010). Although the human brain’s gyrencephalic structure develops in utero and plateaus at birth (Armstrong, Schleicher, Omran, Curtis, & Zilles, 1995; Chi, Dooling, & Gilles, 1977), cortical folding is a dynamic process throughout life which likely reflects the interplay between early neurodevelopmental mechanisms, experience-related reshaping, and neural decline during the course of aging. A number of brain morphometry investigations have shown that prolonged learning and specific trainings impact cortical folding in regions routinely engaged in the learning/training activity. For example, studies on musicians revealed altered morphometric characteristics in the central sulcus (CS) of musicians versus controls (e.g. Bangert & Schlaug, 2006), with a negative association between plastic changes in the CS’ hand area and age of onset of musical training (Li et al., 2009). In other contexts, Luders et al. (2012) compared the degree of folding of long-term meditation practitioners and controls (24–71 years) and revealed a greater gyrification level in meditators’ anterior insula, precentral gyri, right praecuneus and bilateral fusiform gyrus, with a positive association between insular

2. Materials and methods2 2.1. Participants Two-hundred and twelve (n = 212) right-handed adults with no history of neurological or psychiatric condition participated in the study (90 males (M) / 122 females (F); mean age = 35; SD = 19; range = 18–75). The sample comprised 129 bilinguals and 83 monolinguals. Monolinguals were native Italian speakers; bilinguals were Italian-German (n = 27), Dutch-English (n = 17), Hindi-English (n = 32), and Cantonese-English (n = 53) speakers. Education (in years) was collected for all participants (overall mean = 15.36; SD = 3.02). No significant differences in (years of) education were found between bilinguals and monolinguals (t < 1, p > .7). The Mini Mental State Examination (MMSE) (Cockrell & Folstein, 2002) was used 2 The structural Magnetic Resonance Imaging (MRI) and behavioral data used in this study are drawn from the same sample of Del Maschio, Sulpizio, and Fedeli et al. (2019).

2

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to evaluate the cognitive state of participants > 50 years of age (inclusion threshold = ≥ 27 raw score). Mean raw score was 29 (SD = 1.1) and no participant was excluded due to clinical signs of cognitive impairment. No significant differences in MMSE scores were found between bilinguals and monolinguals (t = −1.6; p > .1). For all bilingual speakers, L2 proficiency was measured offline with a picture naming task and an oral translation task from first to second language (see Abutalebi et al., 2014). The naming task comprised 30 coloured pictures taken from a revised version of the Snodgrass and Vanderwart picture set (Snodgrass & Vanderwart, 1980) suitably modified for cultural familiarity and the different L2s spoken. The translation task comprised 66 words controlled for frequency (22 = low frequency; 22 = medium frequency; 22 = high frequency). Second language Age of Acquisition (L2 AoA) was also collected. The descriptive statistics of the overall sample, including linguistic assessment for bilingual participants, are reported in Table 1. The descriptive statistics of the bilingual sample are reported in Table 2. A participants’ subsample (n = 146) with normal or corrected to normal vision performed a revised version of the Flanker task (Fan et al., 2005). 82 participants were bilinguals (mean age = 42.5; SD = 21.76; range = 19–75), 64 were monolinguals (mean age = 36.96; SD = 18.85; range = 18–75). No significant difference in age (t = 0.32; p = .75), education (t = 0.36; p = .72) or MMSE (t = 1.5; p = .13) was detected between bilinguals and monolinguals. Data were collected under the ethical approval of the Human Research Ethics Committees of the Vita-Salute San Raffaele University (Milan, Italy), the University of Hong Kong (HKSAR), and the National Brain Research Centre (Manesar, India).

Table 1 Descriptive statistics of the participants sample, including linguistic assessment for bilingual participants. Mean, standard deviation and range values are reported for Age, Education and Mini-Mental State Examination (MMSE) scores (for participants > 50 years of age). Scores in second language naming (L2 naming accuracy %), first to second language translation (L1 > L2 translation accuracy %), and second language Age of Acquisition (L2 AoA) are reported for bilingual individuals. M = Mean, SD = Standard Deviation, Min-Max = Range.

Age

Education (in years)

MMSE

L2 naming accuracy %

L1 > L2 translation accuracy %

L2 AoA (in years)

M SD Min Max M SD Min Max M SD Min Max M SD Min Max M SD Min Max M SD Min Max

Bilinguals (n = 129)

Monolinguals (n = 83)

35 20.06 19 75 15.4 2.97 6 26 29.15 1.12 27 30 85 10.7 53 100 91.8 8.9 51 100 5.4 3.2 1 18

34.52 17.24 18 75 15.42 2.79 5 25 28.70 1.15 27 30 – – – – – – – – – – – –

2.2. Structural MRI acquisition and image pre-processing T1-weighted MPRAGE images were acquired using 3 T Achieva Philips MR scanners (Philips Medical Systems, Best, Netherlands) at the Vita-Salute San Raffaele (Milan, Italy), the University of Hong Kong (HKSAR) and the National Brain Research Centre (Manesar, India). Identical exam cards were used with the following settings: Repetition time (TR) = 8.03 ms, echo time (TE) = 4.1 ms; flip angle = 8°, field of view (FOV) = 250 × 250, matrix = 256, number of slices = 150, voxel size = 1.0 × 1.0 × 1.0 mm. MRIs were first inspected to exclude the presence of imaging artefacts. Images’ origin was set to match the Anterior Commissure-Posterior Commissure line with SPM12 v6685 (Penny, Friston, Ashburner, Kiebel, & Nichols, 2011). Brain volume segmentation was performed using CAT12 (Gaser & Dahnke, 2016). Structural volumes were segmented into Gray Matter (GM), White Matter (WM) and Cerebrospinal Fluid (CSF). The CAT12 segmentation approach uses a spatial-adaptive non-local means (SANLM) denoising filter (Manjon, Coupe, Marti-Bonmati, Collins, & Robles, 2010) and applies an intensity transformation to bias-correct for regional inhomogeneities and intensity variations (Dahnke, Ziegler, & Gaser, 2012). Additionally, CAT12 jointly uses an Adaptive Maximum A Posterior (AMAP) segmentation (Rajapakse, Giedd, & Rapoport, 1997) and a Partial Volume Estimation (PVE) for a more precise segmentation (Tohka, Zijdenbos, & Evans, 2004). Individual brain volumes were registered to CAT12 inbuilt brain template.

Table 2 Descriptive statistics of the bilingual sample. Mean, standard deviation and range values are reported for Age, Education, Mini-Mental State Examination (MMSE) (for participants > 50 years of age), second language naming (L2 naming accuracy %), first to second language translation (L1 > L2 translation accuracy %), and second language Age of Acquisition (L2 AoA). M = Mean, SD = Standard Deviation, Min-Max = Range.

Age

Education (in years)

MMSE

L2 naming accuracy %

L1 > L2 translation accuracy % L2 AoA (in years)

M SD Min Max M SD Min Max M SD Min Max M SD Min Max M SD Min Max M SD Min Max

ItalianGerman (n = 27)

DutchEnglish (n = 17)

HindiEnglish (n = 32)

CantoneseEnglish (n = 53)

65.3 6.07 52 75 15.4 4.08 7 21 29.5 0.8 28 30 83 10 53 100 91 13 51 100 6 4.19 1 18

21.4 2.03 20 26 15.8 1.1 15 18

22.97 2.32 20 28 16.6 2.04 13 21

–

–

89 6 80 97 97 4 83 100 6.6 2 2 9

92 4 80 97 93 4 84 98 4.75 2.14 2 11

32 18.04 19 75 15.04 2.51 6 22 28.4 1.3 27 30 79 12 57 97 90 10 51 100 5.04 3.47 1 16

2.3. Cortical surface extraction and gyrification parameters calculation The estimation of the cortical surface was conducted on each T1weighted image (n = 212) using the fully-automated CAT12 surface extraction pipeline. With respect to other surface reconstruction software tools (e.g. FreeSurfer), CAT12 provides comparable results in the face of less computational power and processing time required, thus representing a valuable resource when dealing with large participant datasets (Righart et al., 2017; Seiger, Ganger, Kranz, Hahn, & Lanzenberger, 2018). Cortical thickness and central surface reconstruction were jointly computed with Projection-Based Thickness 3

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FWE correction for multiple comparisons.

estimation (PBT) (Dahnke, Yotter, & Gaser, 2013) for both hemispheres of each brain image. Spherical harmonics-based topology correction was applied (Yotter, & Dahnke, et al., 2011) to repair topological defects. The cortical surface mesh was then reparameterized and registered to a template spherical map (Yotter, & Nenadic, et al., 2011). The Gyrification Index (GI) was computed locally as the mean curvature of the cortical surface based on the absolute mean curvature approach as previously described (Luders et al., 2006, 2012). Mean curvature maps were smoothed using a surface-based 25-mm FWHM Gaussian kernel.

2.6. The relationship between gyrification and executive control performance in bilinguals and monolinguals To assess whether executive control performance was differentially modulated by local gyrification in bilinguals and monolinguals, a participants’ subsample (n = 146) performed a revised version of the Flanker Task (Fan et al., 2005), which measures the ability to resolve conflict between competing stimuli and responses. In the Flanker task, a visually presented target (a left-pointing or right-pointing arrow) is flanked by either congruent or incongruent distractors (other arrows with either the same orientation or a different orientation to the target) causing response conflict. Targets presented in congruent conditions (→ →→→→) are generally associated with better performance, that is higher accuracy and lower RTs; targets presented in incongruent conditions (←←→←←) are generally associated with performance decline, that is lower accuracy and increasing RTs. How quickly and/or accurately participants can respond to response-compatible versus -incompatible trials is generally interpreted as an index of conflict resolution ability. For task procedure details, see Del Maschio et al. (2019). A linear mixed-effects model was run (using R software) with Flanker’s Response Times (RTs) as dependent variable and Flanker condition (‘congruent’ vs. ‘incongruent’), GI (as a continuous variable), Language Group (‘monolingual’ vs. ‘bilingual’) and Age (as a continuous variable) as predictors. Gender, Ethnicity and Education (in years) were entered as covariates. By-participants random intercepts were also included.

2.4. Correlation analysis between linguistic measures Preliminary correlation analyses between linguistic measures were run to avoid multicollinearity. Spearman’s correlations were performed between L2 AoA and the two proficiency measures (i.e., L2 naming and L1 > L2 translation). In case two linguistic measures were highly correlated (r > 0.50), only one of them was included in the analyses. 2.5. Neuroimaging analyses 2.5.1. Whole-brain analysis A whole-brain approach was justified by the application of a relatively new neuroimaging analysis technique (i.e., SBM) to an understudied cortical feature in bilingualism and aging research (i.e., gyrification). GI data were entered into a full factorial model with Language Group (‘monolingual’ vs. ‘bilingual’) as factor and Age as a continuous variable. Gender, Ethnicity, Education (in years), Total Intracranial Volume (TIV), and Proficiency (i.e., L2 naming) were entered as covariates. The main effect of Age on GI across the whole cortex was assessed for all participants, independent of Language Group. Directional differences in regression slopes were then computed to investigate interactions between Age and Language Group (Age*bilinguals > Age*monolinguals; Age*monolinguals > Age*bilinguals).

2.7. The relationship between gyrification and L2 Proficiency/L2 AoA in bilinguals To provide additional insights into bilingualism-mediated cortical plasticity, correlation analyses were run between significant GIs and bilinguals’ second language proficiency (i.e., L2 naming and L1 > L2 translation scores) as well as between significant GIs and bilinguals’ AoA. Pearson correlations were used when measures were normally distributed; in the other cases, Spearman correlations were run.

2.5.2. Region of Interest (ROI) analysis A Region-of-Interest (ROI) analysis was conducted to examine differences in cortical regions implicated in bilingual language processing and suffering from early or greater-than-average degradation with increasing age. In particular, cingulo-fronto-parietal structures related to executive control (Abutalebi & Green, 2016) and temporal lobe structures associated with memory functions (e.g. Squire & Zola-Morgan, 1991) were selected. The Desikan–Killiany atlas was used for ROI labelling. GI data were extracted from the following bilateral ROIs:

3. Results 3.1. Neuroimaging results 3.1.1. Whole-Brain Age-related reductions in gyrification were found in dorsolateral and mesial aspects of a widespread network of right frontal and parietal structures, independent of participants’ language group. A significant interaction between Age and Language Group (p < .001; d = 0.0923) showed a preserved degree of gyrification with increasing age in bilinguals’ caudal division of the right ACC (see Table 3). The effect size observed is smaller than those achieved in previous structural MRI studies comparing bilingual and monolingual groups. However, using smaller samples, those studies were more likely to see inflated effects, the accuracy of our test being arguably higher in detecting group differences at the population-level (for a critical discussion, see Munson & Hernandez, 2019).

1. Cingulo-fronto-parietal structures: Lateral orbital frontal cortex; Medial orbital frontal cortex; Rostral-anterior cingulate cortex; Caudal-anterior cingulate cortex; Posterior cingulate cortex; Isthmus – cingulate cortex; Middle frontal gyrus; Inferior frontal gyrus; Inferior parietal cortex. 2. Temporal lobe structures: Superior temporal gyrus; Middle temporal gyrus; Transverse temporal gyrus; Inferior temporal gyrus; Parahippocampal gyrus; Entorhinal cortex; Fusiform gyrus; Temporal pole. GI data were entered into a full factorial model with Language Group (‘monolingual’ vs. ‘bilingual’) as factor and Age as a continuous variable. Gender, Ethnicity, Education (in years), Total Intracranial Volume (TIV), and Proficiency (i.e., L2 naming) were entered as covariates. The main effect of Age on ROIs’ GI was assessed for all participants, independent of Language Group. Directional differences in regression slopes were then computed to investigate interactions between Age and Language Group (Age*bilinguals > Age*monolinguals; Age*monolinguals > Age*bilinguals). In both Whole-brain and ROI analyses, contrasts were estimated with t-tests and results were corrected using a p < .05 threshold with

3.1.2. Region of Interest (ROI) Age-related reductions in gyrification were found in most selected ROIs, with more extended right-sided decrease. A significant interaction between Age and Language Group showed a preserved degree of gyrification with increasing age in bilinguals’ right caudal ACC (p < .001), right Posterior Cingulate Cortex (PCC) (p = .007), and right Entorhinal Cortex (EC) (p = .008) (see Table 4 and Fig. 1). 4

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Table 3 Whole-brain analysis results. Atlas Region (DK40)

Hemisphere

Aging Effect (negative effect of age) Caudal anterior cingulate right Insula right Precentral gyrus right Superior frontal gyrus right Postcentral gyrus left Superior temporal gyrus left Postcentral gyrus right Postcentral gyrus right Age*Bilinguals > Age*Monolinguals Caudal anterior cingulate right Age*Monolinguals > Age*Bilinguals – –

K (in vertices)

p-value (whole-brain FWE corrected)

t

Equiv Z

MNI coordinates (x,y,z)

7029 1063 608 196 384 102 143 166

< .001 < .001 < .001 .001 .001 .002 .02 .011

15.24 8.45 5.93 5.11 5.09 4.97 4.34 4.5

Inf 7.81 5.69 4.95 4.93 4.82 4.24 4.39

4 36 26 5 −18 −41 27 27

15 −26 −9 4 −31 −25 −36 −36

24 7 47 67 73 1 58 58

409

< .001

5.92

5.68

4

19

29

–

–

–

–

–

–

–

Eff. size

CI

0.092

0.055

P < .05 FWE corrected for multiple comparisons, K > 50 vertices spatial threshold.

between Age and PCC was significant for monolinguals (β = 2.21, st. err. = 0.98, t = 2.23, p = .02) but non for bilinguals (t = < 1, p = > .9).

Table 4 Region of Interest (ROI) analysis results. Atlas Region (DK40)

Aging Effect (negative effect of age) Caudal anterior cingulate Isthmus cingulate Lateral orbitofrontal cortex Posterior cingulate Rostral anterior cingulate Fusiform gyrus Medial orbitofrontal cortex Entorhinal cortex Transverse temporal gyrus Parahippocampal gyrus Inferior temporal gyrus Transverse temporal cortex Age*Bilinguals > Age*Monolinguals Caudal anterior cingulate Entorhinal cortex Posterior cingulate Age*Monolinguals > Age*Bilinguals –

p-value (wholebrain FWE corrected)

t

right right right right right right right right right right right left

< .001 < .001 < .001 < .001 < .001 < .001 < .001 < .001 < .001 < .001 < .001 .001

12.90 14.52 9.58 11.28 12.41 8.69 8.67 6.14 5.28 5.17 4.94 4.15

Inf Inf Inf Inf Inf 8.01 7.99 5.88 5.11 5.00 4.79 4.06

right right right

< .001 .008 .009

5.73 3.77 3.71

5.52 3.70 3.65

–

–

–

–

Hemisphere

equivZ

3.3. The relationship between gyrification and L2 Proficiency/AoA in bilinguals A positive correlation for young (S = 82881, p = .005087, r = 0.29) and older adult bilinguals (t = 2.1255, df = 38, p = .0401, r = 0.32) was detected between GI in the right PCC and scores for L2 naming. No significant association was found between GI in the right PCC and scores for L1 > L2 translation. Also, no significant association was found between GI in the right ACC or EC and L2 proficiency (whether L2 naming or L1 > L2 translation scores). No significant associations were found for young adult bilinguals between L2 AoA and GI in the right ACC (S = 120120, p = .83; r = −0.02), right PCC (S = 113770; p = .76; r = 0.03) or right EC (S = 110680; p = .59; r = 0.5). No associations were detected for older adult bilinguals either (right ACC: S = 10764, p = .95, r = −0.01; right PCC: S = 13652, p = .08, r = −0.28; right EC: S = 3624.6, p = .96, r = 0.01). 4. Discussion

P < .05 FWE corrected for multiple comparisons.

An SBM approach was adopted to investigate the contribution of bilingual experience to gyrification from early adulthood to old age in a sample of bilinguals and monolingual controls. Preserved gyrification with increasing age was detected in bilinguals’ right cingulate and entorhinal cortices, regions vulnerable to normal and pathological brain aging. A positive correlation was found for young and older adult bilinguals between gyrification in the right PCC and proficiency in L2 naming.

3.2. The relationship between gyrification and executive control performance in bilinguals and monolinguals The descriptive statistics of participants’ performance on the Flanker task are reported in Table 5. When the GI of the right ACC was used as predictor, the model only showed main effects of Language group (β = 107.83, st. err = 53.24, t = 2.02, p = .04) and Age (β = −5.72, st. err. = 1.47, t = 3.88, p < .001), as well as the classic Flanker condition × Age interaction (β = 2.29, st. err. = 0.70, t = 3.27, p = .001) indicating that performance decline with increasing age was larger in the incongruent condition. When the GI of the right PCC was used as predictor, the model showed a main effect of Age (β = 5.73, st. err. = 1.19, t = 4.80, p = < .001), a main effect of PCC (β = −116.80, st. err. = 39.96, t = 2.92, p = .004), as well as, again, the Flanker condition × Age interaction (β = 1.65, st. err. = 0.55, t = 2.99, p = .003). Moreover, a Language Group × PCC interaction (β = 135.04, st. err. = 54.58, t = 2.47, p = .01), and an Age × PCC interaction (β = 2.55, st. err. = 0.95, t = 2.66, p = .008) emerged as significant. Finally, when we split for Language Group the significant three-way interaction between Language Group, PCC and Age (β = −2.57, st. err. = 1.18, t = −2.17, p = .03), results indicated that the two-way interaction

4.1. Whole-brain analysis Whole-brain analysis revealed age-related cortical changes for all participants, with more significant and extended gyrification reductions in dorsolateral and mesial aspects of frontal and parietal cortices. A larger decrease was detected in the right hemisphere, consistent with the over-recruitment of contralateral regions due to hemispheric asymmetry reduction in response to age-related neural decline (Cabeza, 2002). These findings largely recapitulate previous morphometric accounts of normal gyrification trajectories across the adult lifespan (Hogstrom, Westlye, Walhovd, & Fjell, 2013; Jockwitz et al., 2017; Magnotta et al., 1999). Cortical folding reductions are associated with widening of the cortical sulci and thinning of the gyral crowns, with the subsequent filling-up of freed space by CSF. These changes are likely 5

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Fig. 1. Language Group × Age interaction on Gyrification Index (GI) and correlations with L2 proficiency (Region of Interest level). On the left, the figure displays a mid-sagittal section of the right hemisphere. A preserved degree of gyrification with increasing age was detected in bilinguals’ right caudal Anterior Cingulate Cortex (ACC), right Posterior Cingulate Cortex (PCC), and right Entorhinal Cortex (EC). The color bar encodes significance. On the right, the scatterplots show the positive correlations between GI in the right PCC (y axis) and young and older bilinguals’ scores for second language (L2) naming (x axis).

4.1.2. Right caudal ACC When inspecting for language group differences in gyrification on the entire cortical surface, a preserved degree of cortical folding with increasing age was found in bilinguals’ right caudal ACC, a core component of the executive control network. Located bilaterally in the medial frontal lobes, especially the dorsal aspects of the ACC (dACC) are widely assumed to underpin conflict monitoring and error detection in information processing (Botvinick et al., 1999, 2001; Ridderinkhof, Ullsperger, Crone, & Nieuwenhuis, 2004). While not typically involved in monolingual language processing (e.g. Gitelman, Nobre, Sonty, Parrish, & Mesulam, 2005), the dACC is activated when bilinguals perform both linguistic and non-linguistic conflict tasks (Abutalebi et al., 2012; De Baene, Duyck, Brass, & Carreiras, 2015) as well as during language switching and translation (Abutalebi et al., 2007; Price, Green, & Von Studnitz, 1999). As multiple languages are simultaneously active and compete for attention in the bilingual mind (see Kroll, Dussias, Bogulski, & Kroff, 2012), plastic changes in bilinguals’ ACC are assumed to result from the continuous challenge of monitoring for potential cross-linguistic interference in order to correctly use a target language, especially in demanding languageswitching conditions (Abutalebi & Green, 2007; Green & Abutalebi, 2013). Becker, Prat, and Stocco (2016) used Dynamic Causal Modeling (DCM) on task-related fMRI data to study the mechanisms by which adaptive behavior might be accomplished at the neural-network level in bilingual and monolingual individuals. Differences between groups concerned the magnitude and directionality of the influence of the ACC

Table 5 Participants’ mean latencies (in ms) for correct responses (with standard deviations, SD) in the Flanker task. RT Congruent trials Incongruent trials

Mean SD Mean SD

Bilinguals (n = 82)

Monolinguals (n = 64)

602.87 102.70 710.00 126.05

571.77 133.34 668.40 148.53

driven both by GM and WM decrease (Shen et al., 2018; Symonds, Archibald, Grant, Zisook, & Jernigan, 1999), although the specific contribution of GM and WM to cortical surface atrophy is yet to be fully elucidated. It is likewise unclear whether the effects on sulcal and gyral shape are secondary to mechanical processes such as morphologic shrinkage, result from more active changes in axonal connectivity between regions, or both (Im et al., 2008; Shen et al., 2018). Whilst we did not consider measures of SA and CT in the present study, it has been reported that the physiological decline of local gyrification with increasing age parallels reductions in regional SA, and that both measures are negatively associated with CT (e.g. Gautam et al., 2015; Hogstrom et al., 2013). Such inverse relationship has been proposed to reflect a pattern of regional “cortical stretching” informed by the phylogenetic principle of maximizing SA and gyrification rather than CT in order to optimize connectivity and functional specialization of the cortex (Hogstrom et al., 2013; see also Toro & Burnod, 2005). 6

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declarative systems in aging is currently mixed. Whereas some studies reported even more damage for older adult bilinguals versus monolingual controls (both healthy and diseased) in memory-related structures (Gold et al., 2013; Schweizer, Ware, Fischer, Craik, & Bialystok, 2012), other studies found greater GMV in the left temporal pole for older bilinguals (Abutalebi et al., 2014), greater GMV in the left hippocampus for older bimodal bilinguals (Li et al., 2017), and an anticorrelation between temporal pole thickness and age exclusive to older monolinguals (Olsen et al., 2015). To our knowledge, the finding here reported of a preserved degree of folding in the right EC is the first instance of bilingualism-mediated plasticity in this particular region. Inconsistencies in the literature may be due to methodological differences, and highlight the importance of investigating quantitative features of cortex structure and morphology separately.

on other key regions of the executive control network (i.e., dorsolateral prefrontal cortex (DLPFC) and striatum). These findings have been proposed to reflect a different way in which the executive control network handles conflicting information detected by the ACC, possibly resulting from a different adaptation of conflict response mechanisms in bilinguals and monolinguals. Our whole-brain results suggest that cumulative bilingual experience significantly counteracts physiological atrophy in the caudal ACC, and extend previous gray matter findings of larger GMV in the same region for both young and older bilinguals relative to monolingual controls (Abutalebi et al., 2012, 2015). 4.2. Region of Interest (ROI) analysis ROI analysis on cingulo-fronto-parietal and temporal lobe structures revealed heterogeneous patterns of age-related cortical changes for all participants, with a more significant gyrification decrease in the right hemisphere. When inspecting for language-group differences in ROIs’ gyrification across age, we found that cumulative bilingual experience significantly counteracts physiological surface atrophy in the right caudal ACC, the right PCC and the right EC.

4.3. The relationship between gyrification and L2 Proficiency/AoA in bilinguals A positive correlation was found both in young and older adult bilinguals between degree of gyrification in the right PCC and L2 naming accuracy. Although the unreached consensus about the functional role of the PCC does not allow us to rule out alternative interpretations, this finding seems to indicate that the establishment and control of an L2 lexico-semantic system has early, long-lasting, and proficiency-dependent effects on posterior cingulate gyrification. It has been posited that the co-activation of the PCC with the DLPFC underlies the ability to perform semantic decisions of varying difficulty, and shown that the functional coupling at rest between these regions is stronger for participants who are more efficient at semantic tasks judgements (KriegerRedwood et al., 2016). Recently, a proficiency-mediated recruitment of the right PCC in a picture-word matching task has been documented in young adult bilinguals (Nichols & Joanisse, 2016). An association between functional engagement of the PCC and language proficiency has also been reported by Briellmann et al. (2004), who administered to multilingual participants a task that required to generate verbs from semantically related nouns. Whereas proficiency modulated the degree of activation within frontotemporal areas of the language network, a deactivation of the PCC was found as proficiency decreased. The authors suggested that this would reflect allocation of resources to more anterior systems in order to accommodate the higher cognitive load associated with lower proficiency. Notably, no significant associations were found for both young and older adult bilinguals between ROIs’ gyrification and L2 AoA. Previous evidence has shown that both plasticity and variability in L2 attainment are conditioned by L2 AoA (see Birdsong, 2018), and that the age when L2 learning begins can modulate the relationship between genetic variants associated with cognitive flexibility in adulthood and bilingual proficiency (Vaughn & Hernandez, 2018). However, it is also well known that the brain can continually reconfigure its structure and function as a result of knowledge or skill acquisition beyond time windows of higher plasticity (i.e., early developmental stages), as reflected in changes in GM and connectivity in late L2 learners (Li, Legault, & Litcofsky, 2014; Rossi, Cheng, Kroll, Diaz, & Newman, 2017). Our data suggest that the preserved degree of gyrification in the cingulate cortex relates to proficiency rather than AoA. Overall, the present study should be considered in light of a number of limitations. Among others, the lack of Socio-Economic Status (SES) and language usage variables. The neurocognitive relevance of these variables is well-known. As a partial compensation, education and ethnicity have been entered as covariate in all our models. Previous morphometric studies have reported global and regional differences in brain structure between Caucasian and Asian populations (Kochunov et al., 2003; Uchiyama, Seki, Tanaka, & Koeda, 2013). However, the effect of ethnic disparities on gyrification indices is largely unknown. The available evidence nonetheless indicates that cortical measures associated with gyrification such as regional sulcation pattern and

4.2.1. Right PCC Located posterior to the ACC on the brain’s midline, the PCC is a highly connected structure which has been shown to serve multiple functional roles across cognitive, emotional and sensorimotor domains (Leech & Sharp, 2013; Vogt, Vogt, & Laureys, 2006). Accordingly, the interpretation of our structural finding can only be tentative. The PCC is strongly connected to different networks involved in attentional control such as the dorsal attentional network and the frontoparietal control network. Based on extensive experimental and clinical data, Leech and Sharp (2013) have indicated the PCC as critical in supporting the control of attentional focus. Within the bilingualism realm, the activation of the PCC has been reported during non-verbal conflict tasks in bilingual children (Mohades et al., 2014) and verbal switching tasks in young bilingual adults (Reverberi et al., 2015; Weissberger, Gollan, Bondi, Clark & Wierenga, 2015). de Bruin, Roelofs, Dijkstra, & FitzPatrick (2014) documented that switching out of the first language into a weaker language increased activation in the right PCC and other areas related to language control. Most recently, Green (2019) explored the relationship between language control in bilinguals and attentional states during a conversation, and assigned a key role to the PCC in mediating transitions between attentional states for both the processing of conversational topics and global and local language control conditions. Our finding of preserved PCC gyrification with increasing age exclusive to bilinguals can thus be interpreted by emphasizing the purported role of this structure in the regulation of attentional states in response to context-dependent changes. Further experimental indication is needed to confirm this interpretation. 4.2.2. Right EC The earliest stages of Alzheimer’s disease (AD) are thought to develop within medial temporal lobe (MTL) structures such as the EC (Braak & Braak, 1991), a parahippocampal region which interfaces the neocortex and the hippocampal formation and is crucially involved in memory functions (Preston & Eichenbaum, 2013). EC degradation has also been reported in semantic dementia (Chan et al., 2001; Davies, Graham, Xuereb, Williams, & Hodges, 2004), characterized by loss of (verbal) semantic knowledge. For the successful learning of a second language, an extensive array of (word)form-meaning mappings largely distinctive from L1 must be stored in MTL structures, suggesting that the neural instantiation of a complex lexico-semantic repertoire may contribute to build-up neural reserve therein. However, even if training studies on young adults demonstrated neuroplastic changes in MTL regions such as the hippocampus as a function of L2 lexical development (e.g. Bellander et al., 2016; Mårtensson et al., 2012), evidence pointing to bilingualism as a neuroprotective factor to MTL-based 7

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surface area are not influenced by ethnic group membership, both in infants (Jha et al., 2018) and adults (Del Maschio et al., 2019; Wei et al., 2017). With regard to language use, we can speculate that our bilingual participants used two languages on a daily basis, given that all bilinguals lived in highly immersive bilingual environments such as South Tyrol – where Italian and German are official languages –, Honk Kong – where Cantonese and English are official languages –, and Manesar (India) – where Hindi and English are official languages. It was also impossible to control for the physical and social components of participants’ leisure activities. A further limitation is that some of our bilingual participants (i.e., the Cantonese-English subgroup) spoke a tonal language as L1. As lexical tone processing recruits – among other structures – a ventral auditory stream encompassing the aSTG (see Liang & Du, 2018), we cannot rule out the possibility that language group differences in the MTL are partially driven by the distinctive properties of Cantonese phonology.

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5. Conclusions The findings here reported may be profitably framed within (neuro) emergentist models representing bilingualism as a non-linear system arising from the dynamic interaction of smaller elements across time (e.g. Hernandez, Li, & MacWhinney, 2005; Hernandez et al., 2019). According to these models, the complexity of language should be understood in terms of the interaction of more basic non-linguistic factors, such as perceptual mechanisms, working memory and processing capacity, as well as characteristics of environmental experience. First, in accordance with a basic principle of these approaches, our finding of cortical plasticity in the cingulate and entorhinal cortices suggests that experience with two languages does more than alter the neural substrate strictly responsible for language processing, subtending a substantial degree of interactivity between language and other cognitive systems. Second, the preserved degree of gyrification exclusive to older bilinguals may be interpreted as indicating that bilingualism is an iterative process which requires time for language experience and general cognition to interact and bolster cortical systems. 6. Statement of Significance We used Surface-based Morphometry to investigate for the first time the contribution of bilingual experience to gyrification from early adulthood to old age in a sample of bilinguals and monolingual controls. Our results provide novel insights on experience-related cortical reshaping and bilingualism-induced cortical plasticity across adult lifespan. Declaration of Competing Interest None. Acknowledgements We thank Prof. Christian Gaser for his technical support. Appendix A. Supplementary material Supplementary data to this article can be found online at https:// doi.org/10.1016/j.bandl.2019.104680. References Abutalebi, J., & Green, D. (2007). Bilingual language production: The neurocognition of language representation and control. Journal of Neurolinguistics, 20(3), 242–275. https://doi.org/10.1016/j.jneuroling.2006.10.003. Abutalebi, J., & Green, D. W. (2016). Neuroimaging of language control in bilinguals: Neural adaptation and reserve. Bilingualism: Language and Cognition, 19, 689–698. https://doi.org/10.1017/S1366728916000225.

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