Elsevier

NeuroImage

Volume 83, December 2013, Pages 66-74
NeuroImage

Cortical thickness asymmetry from childhood to older adulthood

https://doi.org/10.1016/j.neuroimage.2013.06.073Get rights and content

Highlights

  • Cortical thickness decreased with age in 274 5-59 year old healthy participants.

  • Children showed regions of cortical asymmetry in vision and language areas.

  • Cortical thickness asymmetry increased with aging in frontal and parietal lobes.

Abstract

Age-related thinning of the cortical mantle varies regionally, leading to hemispheric asymmetries in cortical thickness that may emerge at various stages of development and aging. Cortical asymmetry may play a role in modulating the functional maturation (or degradation) of language and cognition in humans, but its evolution over the lifespan is unknown. Here cortical thickness was negatively correlated with age in 274 5–59 year old, right-handed healthy participants. Pre-adolescents showed limited regions of cortical asymmetry focused on medial occipital lobe (R > L) and inferior frontal gyrus (R > L), namely vision and language relevant areas. More extensive frontal (lateral R > L, medial L > R) and parietal lobe (lateral L > R, medial R > L) asymmetries emerged after adolescence, and increased during aging. Changes of cortical asymmetry in these regions may be linked to specialization of the brain with maturity.

Introduction

Hemispheric asymmetry in the human brain, particularly in cortical gray matter, is associated with language, motor and cognitive functions and may depend on a variety of factors related to heredity, development and pathology (Toga and Thompson, 2003). It has been observed, initially from autopsy and later from imaging, that the frontal right hemisphere protrudes more anteriorly and is often wider than the left, and the left occipital lobe extends beyond and is often wider than the right in many individuals, so-called “Yakovlevian torque” (LeMay, 1976, Toga and Thompson, 2003). This asymmetry extends to the thickness of the cortex, measured from in vivo T1-weighted magnetic resonance images (MRI) as the distance between the pial–cortical surface and gray–white matter surface (MacDonald et al., 2000), that differs in analogous regions of the left and right hemispheres in healthy young adults (Luders et al., 2006). This structural morphology reflects differences of gray matter volume (Takao et al., 2011, Tanaka et al., 2012, Weinberger et al., 1982) and cortical thickness (Luders et al., 2006) in frontal (greater in the right), middle (greater in the left planum temporale) and occipital regions (greater in the left). The pattern of cortical asymmetry may inform about specific structural abnormalities linked to functional deficits associated with psychiatric (e.g. schizophrenia) and neurological (e.g. Alzheimer's) disease (Haller et al., 2009, Hamilton et al., 2007, Kim et al., 2012, Li et al., 2012, Long et al., 2012, Shaw et al., 2009). Although cortical asymmetry was not explicitly assessed versus human intelligence, there are some studies that have looked at relationships between cortical thickness and IQ which have found significant correlations that differed between hemispheres (Choi et al., 2008, Karama et al., 2011, Narr et al., 2007, Shaw et al., 2006, Yang et al., 2013).

Cortical asymmetry can develop as a result of hemispheric counterparts not maturing at the same time, causing structural and functional asymmetries important for specialization and operational efficiency. From childhood to adulthood, the brain matures with a process of progressive myelination (Benes et al., 1994) and synapse elimination (Bourgeois and Rakic, 1993, Huttenlocher and Dabholkar, 1997). Myelination progresses from inferior to superior and posterior to anterior: the brain stem and cerebellum are myelinated first, followed by occipital, parietal and temporal cerebral areas, and lastly the frontal lobes (Benes et al., 1994). Patterns of cortical thinning, as measured on MRI, are in line with those of myelination: parietal and occipital areas exhibit greater thickness decreases than other regions during childhood to young adulthood (Sowell et al., 2004, Tamnes et al., 2010, van Soelen et al., 2012); while frontal and temporal areas show more age-related change from young to older adulthood (Fjell et al., 2009, Lemaitre et al., 2012, Westlye et al., 2010). As a result of bilateral cortical maturity, the asymmetry of regional gray matter volume, which is present at birth (Gilmore et al., 2007), undergoes a developmental progression in childhood and adolescence (Giedd et al., 1996, Reiss et al., 1996). The leftward asymmetry in the occipital region seen at birth (Gilmore et al., 2007) appears preserved at adolescence (Giedd et al., 1996, Reiss et al., 1996), while rightward asymmetry of prefrontal areas in children and adolescents (Giedd et al., 1996, Reiss et al., 1996) emerges from symmetric volumes at birth (Gilmore et al., 2007). The cortical asymmetry has shown alterations in childhood neurological disorders, such as autism (Herbert et al., 2005) or prenatal alcohol exposure (Sowell et al., 2002). Only one study has investigated typical developmental trends of cortical thickness asymmetry, specifically over an age range of 3–22 years (Shaw et al., 2009). Relative to the contra-lateral hemisphere, the left inferior frontal and the right occipital–parietal areas were thicker in healthy children, but there was an inversion of this asymmetry pattern after adolescence.

However, the progression of cortical thickness asymmetry throughout the lifespan is unknown. In addition to charting the typical development and aging profile for use as a baseline to better understand clinical disorders, observed structural changes in cortical asymmetry may underpin developmental milestones in specialization of brain regions (Jung and Haier, 2007). In the current cross-sectional study, we investigate patterns of cortical maturation and asymmetry in 274 healthy subjects over a wide age range of 5 to 59 years to determine the trajectory of cortical asymmetry in healthy development and aging from childhood to older adulthood.

Section snippets

Participants and imaging

Participants for this study were 274 healthy (150 females/124 males), right-handed individuals aged 5–59 years recruited from the Edmonton area. Original recruitment pooled 288 participants, but only scans of right handed participants with good quality of images (visual inspection and CIVET quality control) were analyzed in the current study. Health of participants was verified by asking a series of questions to ensure there was no history of neurological or psychiatric disease or brain injury.

Regional decrease in cortical thickness with age

Mean cortical thickness in our six age groups (Group 1: 5–9 years, n = 45, 22 females; Group 2: 10–14 years, n = 41, 22 females; Group 3: 15–19 years, n = 47, 24 females; Group 4: 20–29 years, n = 51, 28 females; Group 5: 30–39 years, n = 51, 25 females; Group 6: 40–59 years, n = 46, 29 females) is shown in Fig. 1. Thickness patterns were similar across all the age groups, with greatest thickness observed in bilateral insula, temporal lobe, temporal pole and medial frontal lobe, and the thinnest cortex in the

Discussion

In this study, hemispheric differences in cortical thickness were observed to change with age. There was an interesting dichotomy of asymmetry patterns between the frontal and posterior parts of the brain. In the frontal part of the brain, the left lateral vertices were thinner than the right, and the left medial vertices were thicker. Conversely, in the posterior part of the brain, left lateral vertices were thinner and left medial vertices were thicker than their right hemisphere

Acknowledgments

We thank the Canadian Institutes of Health Research (CIHR) and the Networks of Centres of Excellence (CLLRNet) for operating; Alberta Innovates — Health Solutions (CB) and Natural Sciences and Engineering Research Council (CL) for salary; and Sarah Treit for useful comments on the manuscript.

Conflict of interest

None.

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    1

    Postal address: Department of Biomedical Engineering, 1098 Research Transition Facility, University of Alberta, Edmonton, AB T6G 2V2, Canada.

    2

    Postal address: Research Unit, Alberta Children's Hospital, 2888 Shaganappi Trail NW, Calgary, Alberta T3B 6A8, Canada.

    3

    Postal address: McConnell Brain Imaging Center, Montreal Neurological Institute, McGill University, Montreal, Quebec, Canada.

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