Elsevier

NeuroImage

Volume 56, Issue 3, 1 June 2011, Pages 865-873
NeuroImage

The relationship between cortical sulcal variability and cognitive performance in the elderly

https://doi.org/10.1016/j.neuroimage.2011.03.015Get rights and content

Abstract

The relationship between cognitive functions and brain structure has been of long-standing research interest. Most previous research has attempted to relate cognition to volumes of specific brain structures or thickness of cortical regions, with relatively few studies examining other features such as cortical surface anatomy. In this study, we examine the relationship between cortical sulcal features and cognitive function in a sample (N = 316) of community-dwelling subjects aged between 70 and 90 years (mean = 78.06 ± 4.75; male/female = 130/186) who had detailed neuropsychological assessments and brain MRI scans. Using automated methods on 3D T1-weighted brain scans, we computed global sulcal indices (g-SIs) of the whole brain and average sulcal spans of five prominent sulci. The g-SI, which reflects the complexity of sulcal folds across the cerebral hemispheres, showed a significant positive correlation with performance in most cognitive domains including attention/processing speed, memory, language and executive function. Regionally, a negative correlation was found between some cognitive functions and sulcal spans, i.e. poorer cognitive performance was associated with a wider sulcal span. Of the five cognitive domains examined, the performance of processing speed was found to be correlated with the spans of most sulci, with the strongest correlation being with the superior temporal sulcus. Memory did not show a significant correlation with any individual sulcal index, after correcting for age and sex. Of the five sulci measured, the left superior temporal sulcus showed the highest sensitivity, with significant correlations with performances in all cognitive domains except memory, after controlling for age, sex, years of education and brain size. The results suggest that regionally specific sulcal morphology is associated with cognitive function in elderly individuals.

Research highlights

► We examined 3D cortical sulci of healthy elderly in multiple cognitive domains. ► Sulcal complexity was associated with better cognitive functions. ► Processing speed showed the largest range of correlations with sulcal measures. ► No significant relationship between sulcal morphology and memory was found.

Introduction

Attempts to relate brain structure to function have a long history, going back to the time of phrenology. Recent investigations have used advanced statistical techniques such as regional brain volumetrics or voxel-based morphometry (VBM) to examine the relationship. Positive correlations between brain structure and cognitive functions have been found, such as processing speed (Kochunov et al., 2010, Tisserand et al., 2000), executive function (Newman et al., 2007) and memory (Tisserand et al., 2000) in cognitively healthy adults. However, the studies have not always been consistent, and some surprising negative correlations have been reported, such as better memory being associated with smaller hippocampal volumes in healthy adults in one study (Van Petten, 2004). Furthermore, a review of the literature on structure–function correlations in aging suggested that “the magnitude of the observed associations is modest” (Raz and Rodrigue, 2006).

Quantification of the morphology of the fold on the cortical surface may be helpful in understanding the relationships between brain structure and function. The pattern of sulcal folds, the principal anatomical landmarks of the human cerebral cortex on the brain surface, exhibits its structural complexity (Welker, 1988) and reflects the underlying connectivity (Van Essen, 1997). In addition, it has been shown that the cortical folding patterns can predict cytoarchitecture beyond what was traditionally expected (Fischl et al., 2008). A review paper suggested that the fold geometry was a macroscopic probe for hidden architectural organization or developmental events (Mangin et al., 2010). Further, previous studies pointed out an advantage of sulcal model-based analysis using the contrast between gray matter (GM) and cerebrospinal fluid (CSF), which unlike the contrast between GM and white matter (WM), remains stable in older subjects (Im et al., 2008, Kochunov et al., 2005). In recent studies of sulcal-based analysis, it was found that folding patterns were modified in psychiatric syndromes and neurological disorders including Alzheimer's disease (Im et al., 2008, Mega et al., 1998), schizophrenia (Cachia et al., 2008) and bipolar disorder (Penttila et al., 2009). Furthermore, morphological difference of sulci had been found in certain professional groups, such as musicians (Li et al., 2009).

The first attempt to quantify the extent of the cortical folding relied on the gyrification index, namely, the ratio of the total pial cortical surface over the perimeter of the brain delineated on two-dimensional slices (Armstrong et al., 1995, Cachia et al., 2008, Luders et al., 2004, Zilles et al., 1988). Recently a new index of sulcal folds, called the global sulcal index (g-SI), has been computerized as a three-dimensional (3D) version of the gyrification index globally. The g-SI has shown a capacity for being a good biomarker in many studies (Mangin et al., 2010), for example, in detecting abnormalities in early-onset schizophrenia (Penttila et al., 2008) and intermediate-onset bipolar disorder (Penttila et al., 2009, Penttilä et al., 2009). The width of cortical sulci, called the sulcal span, has been proposed as another measure. Several studies have found that the width of cortical sulci expands linearly with aging from early adulthood to old age (Liu et al., 2010, Kochunov et al., 2005, Magnotta et al., 1999). Additionally, developmental abnormalities of cortical sulci in bipolar disorder were observed by examining the width of sulci (Coyle et al., 2006). A recent study also found that the average sulcal span in the frontal lobe was negatively associated with processing speed in 38 healthy elderly individuals (Kochunov et al., 2010).

In the present study, we investigate the relationship between cognitive function and global/regional sulcal morphometry based on the cortical surface of non-demented community-dwelling individuals in the age range of 70–90 years by examining the correlations between a range of neuropsychological domains (including attention/processing speed, memory, language, executive function and visuospatial ability) and sulcal features (including global sulcal index and five regional sulcal spans). To our knowledge, this is the first study to examine 3D cortical sulcal patterns in community-dwelling elderly with multiple cognitive domains. In a previous study, we reported that age was correlated with the sulcal pattern (Liu et al., 2010). In addition, age has been correlated with cognitive functions, and advancing age is generally accompanied by a decline in some cognitive functions (O'Sullivan et al., 2001). Therefore, we hypothesized that: i) poorer cognitive function will be associated with wider sulcal span and lower g-SI; ii) the sulcus–performance associations are only partially mediated by age, that is correlations between cognitive functions and sulcal features will be present after correcting for age effects; iii) processing speed, which shows the most consistent age-related decline (Salthouse, 1996, Tisserand et al., 2000), would have the most robust relationship with the global sulcal index and sulcal span; iv) there is regional specificity in the relationships, e.g. executive function with the superior frontal sulcus, language with the superior temporal sulcus, and visuospatial function with the intra-parietal sulcus; and v) we suspected that memory may not show a relationship with any of the sulci examined as the organs of memory are subcortical and are not reflected in these sulci.

Section snippets

Subjects

Participants were drawn from Wave 1 of the Sydney Memory and Aging Study (MAS), a prospective study examining the predictors of cognitive decline in an elderly, non-demented, community-dwelling sample. They were recruited randomly from the electoral rolls of two electorates of Eastern Sydney, Australia. Registration on the electoral roll is compulsory for Australian citizens. Participants were excluded from the study if they had been diagnosed as having any of the following: dementia, mental

Results

We found that g-SI significantly decreased with advancing age (F (1, 622) = 5.822, p = 0.016) and the widths of all five sulcal spans increased significantly with age (Wilks's Lambda = 0.830, F (6, 620) = 21.134, p < 0.001,), after controlling for sex, ICV, scanner and hemisphere. Therefore, to investigate the correlations between cognitive function and sulcal features, we treated age as a covariate on the change of sulcal morphology.

Globally, partial correlation analysis showed that there were positive

Discussion

The aim of the current study was to examine the relationship between cognitive function and the fold geometry of a set of sulcal regions in an elderly population. It has previously been shown that advancing age leads to an increase in the widths of sulci and a decrease in g-SI (Kochunov et al., 2005, Liu et al., 2010), as well as a decline in neuropsychological performances (O'Sullivan et al., 2001). Age-related cognitive changes in the elderly are possibly related to age-related brain

Conclusion

We report widespread correlations of cortical surface anatomy, especially in the frontal and temporal regions, with cognition in non-demented elderly individuals. To our knowledge, this is the first study to examine 3D cortical sulcal patterns in healthy elderly with multiple cognitive domains. The salient findings are that processing speed has a broad and dispersed range of correlations with the cortical surface, with the strongest correlation being with the superior temporal sulcus, while no

Acknowledgments

This research was supported by the National Health and Medical Research Council (NHMRC Program Grant ID 350833 and NHMRC Project Grant ID 510175), the Australian Research Council (DP0774213, DP0773584 and LP0669645). We thank the study participants and interviewers. We also thank Ms. Angie Russell for her assistance in the manuscript preparation, and Laboratoire de Neuroimagerie Assistée par Ordinateur (LNAO) and Dr. Jean-François Mangin for their software BrainVisa and helpful advice.

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