The relationship between cortical sulcal variability and cognitive performance in the elderly
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.
References (74)
- et al.
Voxel-based morphometry—the methods
Neuroimage
(2000) - et al.
A parametric fMRI study of overt and covert shifts of visuospatial attention
Neuroimage
(2001) Problems of test construction in the field of aphasia
Cortex
(1967)- et al.
Cortical folding abnormalities in schizophrenia patients with resistant auditory hallucinations
Neuroimage
(2008) - et al.
Cognitive function and brain structure correlations in healthy elderly East Asians
Neuroimage
(2009) - et al.
Frequency of hippocampal formation atrophy in normal aging and Alzheimer's disease
Neurobiol. Aging
(1997) - et al.
An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest
Neuroimage
(2006) - et al.
Relationship between information processing speed in temporal lobe epilepsy and white matter volume
Epilepsy Behav.
(2004) - et al.
"Mini-mental state". A practical method for grading the cognitive state of patients for the clinician
J. Psychiatr. Res.
(1975) - et al.
Spatial maps in frontal and prefrontal cortex
Neuroimage
(2006)
Parietal and superior frontal visuospatial maps activated by pointing and saccades
Neuroimage
Sulcal morphology changes and their relationship with cortical thickness and gyral white matter volume in mild cognitive impairment and Alzheimer's disease
Neuroimage
A longitudinal study of neurocognitive function in individuals at-risk for psychosis
Schizophr. Res.
Fractal dimension analysis of the cortical ribbon in mild Alzheimer's disease
Neuroimage
Processing speed is correlated with cerebral health markers in the frontal lobes as quantified by neuroimaging
Neuroimage
The effects of age and sex on cortical sulci in the elderly
Neuroimage
A framework to study the cortical folding patterns
Neuroimage
Which brain regions are critically involved in the retrieval of old episodic memory?
Brain Res. Brain Res. Rev.
Spatial cognition: where we were and where we are
Neuroimage
Global and temporal cortical folding in patients with early-onset schizophrenia
J. Am. Acad. Child Adolesc. Psych.
Differential aging of the brain: patterns, cognitive correlates and modifiers
Neurosci. Biobehav. Rev.
Automatic recognition of cortical sulci of the human brain using a congregation of neural networks
Med. Image Anal.
Age-related differences in activation–performance relations in delayed-response tasks: a multiple component analysis
Cortex
The relation between global and limbic brain volumes on MRI and cognitive performance in healthy individuals across the age range
Neurobiol. Aging
Relationship between hippocampal volume and memory ability in healthy individuals across the lifespan: review and meta-analysis
Neuropsychologia
Meta-analyzing left hemisphere language areas: phonology, semantics, and sentence processing
Neuroimage
The topography of white matter hyperintensities on brain MRI in healthy 60- to 64-year-old individuals
Neuroimage
Executive function and the frontal lobes: a meta-analytic review
Neuropsychol. Rev.
The ontogeny of human gyrification
Cereb. Cortex
Controlling the false discovery rate—a practical and powerful approach to multiple testing
J R Stat Soc B Stat Methodol
Der Benton Test
Neural plasticity in the ageing brain
Nat. Rev. Neurosci.
Cortical sulci and bipolar disorder
Neuroreport
Functional MRI during word generation, using conventional equipment: a potential tool for language localization in the clinical environment
Neurology
Automatically parcellating the human cerebral cortex
Cereb. Cortex
Cortical folding patterns and predicting cytoarchitecture
Cereb. Cortex
Examination of processing speed deficits in multiple sclerosis using functional magnetic resonance imaging
J. Int. Neuropsychol. Soc.
Cited by (39)
Neuroanatomical foundations of delayed reward discounting decision making II: Evaluation of sulcal morphology and fractal dimensionality
2022, NeuroImageCitation Excerpt :While the effects of SM on cognition have not been explicitly studied to our knowledge, changes likely reflect reduced size or density of cells, which correlate to cognitive changes in certain conditions, such as multiple sclerosis (Liu et al, 2014). Interestingly, sulcal widening has been previously linked to lowered cognitive performance (Liu et al., 2011), however, in the current study, sulcal widening was associated with lower delay discounting. This conflicts with abundant research linking lowered delay discounting to increased cognitive ability (Shamosh and Gray, 2008).
Structural brain characteristics and gene co-expression analysis: A study with outcome label from normal cognition to mild cognitive impairment
2022, Neurobiology of Learning and MemorySulcal morphology as cognitive decline predictor in older adults with memory complaints
2022, Neurobiology of AgingHigh-density lipoprotein-cholesterol and neuroaging: Memory and gyrification of the insular and frontal opercular cortex
2021, Factors Affecting Neurological Aging: Genetics, Neurology, Behavior, and DietEffects of Statins on Memory, Cognition, and Brain Volume in the Elderly
2019, Journal of the American College of CardiologyCitation Excerpt :Gray matter (GM), white matter (WM), cerebrospinal fluid, and intracranial volume were measured. Total brain volume was defined as the sum of GM and WM. To ensure that no error was introduced by scanner change, 5 participants were imaged on both scanners within 2 months; GM, WM, cerebrospinal fluid, and intracranial volume were similar between the 2 instruments (50). Regional GM volumes were calculated using 90 parcellations, delineated by the Automated Anatomical Labelling atlas (51) using voxel-based morphometry approach (52) (Statistical Parametric Mapping software; Wellcome Department of Imaging Neuroscience, London, United Kingdom).