Using sulcal and gyral measures of brain structure to investigate benefits of an active lifestyle

Highlights

• We examined physical activity, brain structure, and cognition in 318 adults.

• Higher physical activity was associated with brain structure (larger sulcal width).

• Physical activity was not associated with grey matter volume or sulcal depth.

• ROIs associated with physical activity were negatively associated with cognition.

• Sulcal width is a more sensitive marker of physical activity than cortical volume.

Abstract

Background

Physical activity is associated with brain and cognitive health in ageing. Higher levels of physical activity are linked to larger cerebral volumes, lower rates of atrophy, better cognitive function and a lower risk of cognitive decline and dementia. Neuroimaging studies have traditionally focused on volumetric brain tissue measures to test associations between factors of interest (e.g. physical activity) and brain structure. However, cortical sulci may provide additional information to these more standard measures.

Method

Associations between physical activity, brain structure, and cognition were investigated in a large, community-based sample of cognitively healthy individuals (N = 317) using both sulcal and volumetric measures.

Results

Physical activity was associated with narrower width of the Left Superior Frontal Sulcus and the Right Central Sulcus, while volumetric measures showed no association with physical activity. In addition, Left Superior Frontal sulcal width was associated with processing speed and executive function.

Discussion

These findings suggest sulcal measures may be a sensitive index of physical activity related to cerebral health and cognitive function in healthy older individuals. Further research is required to confirm these findings and to examine how sulcal measures may be most effectively used in neuroimaging.

Introduction

It is well established that physical activity (PA) is associated with healthier brain structure (Erickson et al., 2010), better cognitive function (Colcombe et al., 2003), as well as a reduced risk of cognitive decline (Etgen et al., 2010, Muscari et al., 2010) and dementia (Ahlskog et al., 2011). The ageing process is associated with a decline in neurogenesis and an increase in neuroinflammation, which may result in reduced grey matter thickness (Kochunov et al., 2013). Suggested mechanisms contributing to the benefit of PA for cerebral health and cognitive function include: improved cardio-vascular health and cerebral perfusion, decreased chronic low-grade systemic inflammation, activation of anti-oxidant pathways that mitigate the impact of oxidative stress on the brain, and increased neuroplasticity (Anderson-Hanley et al., 2012, Gerecke et al., 2013, Kochunov et al., 2013, Muscari et al., 2010, Radak et al., 2008). In addition, PA provides a safe way (one not associated with increased cancer incidence) to upregulate adult stemcell neurogenesis pathways which has been demonstrated to lead to larger hippocampal volumes in older adults (Erickson et al., 2011).

Higher levels of PA are associated with improved attention, motor function, processing speed, executive function and memory both in intervention trials as well as animal studies (Angevaren et al., 2008, Colcombe et al., 2003, Smith et al., 2010, Stranahan et al., 2012, van Praag et al., 1999). Consistent findings have also been demonstrated in observational studies using cross-sectional and longitudinal designs (Bielak et al., 2007). In addition, research has also linked higher levels of PA with increased grey and white matter volumes in the parietal, prefrontal, and temporal cortex (Colcombe et al., 2006, Erickson et al., 2010, Erickson et al., 2012, Honea et al., 2009, Taubert et al., 2011). These brain regions also underlie executive function, working and episodic memory, and attention, and are implicated in cognitive decline and neurodegenerative disease prevalent in ageing (Colcombe et al., 2004, Erickson et al., 2009, Rosano et al., 2010). These findings have been supported by animal studies demonstrating that PA induces increased neurogenesis and cell connectivity, in turn improving cognitive performance (van Praag et al., 1999).

To date, imaging research investigating risk and protective factors for cerebral health has focused on examining volumetric measures of brain structure (Lemaitre et al., 2012). Despite the value of such findings, these techniques have several limitations. First, volumetric techniques rely on the ability to accurately identify grey and white matter boundaries. However, grey–white matter signal contrast on MRI decreases with age and leads to increased variability of measurement, over-estimation of white and under-estimation of grey matter volumes thus resulting in reduced sensitivity of these measures in older adults (Kochunov et al., 2005, Lemaitre et al., 2012). Second, they may be less sensitive to more diffuse processes affecting cortical regions that do not necessarily follow clear anatomical boundaries or rely on sub-processes spread across adjoining gyri (Van Essen, 1997). Thirdly, many cerebral functions are affected concurrently by changes in both grey and white matter integrity which may not be optimally indexed by volumetric measures at the local level (Kochunov et al., 2005).

An alternative or potentially complementary approach to examining grey and white matter is the analysis of cortical sulci (Kochunov et al., 2005, Lemaitre et al., 2012). While cortical sulcal width increases with age (Kochunov et al., 2005), narrower sulcal width is associated with higher cognitive function (Liu et al., 2011). In addition, cortical sulcal depth reduces with age and pathological cognitive decline (e.g. Alzheimer's disease) (Im et al., 2008, Kochunov et al., 2005). Therefore, healthier sulci are characterised by narrower width and greater depth (Im et al., 2008, Liu et al., 2011). Examining characteristics of cortical sulci thus provides a sensitive representation of brain structure, which is not reliant on the discrimination of grey and white matter yet indexes atrophy in both (Kochunov et al., 2005), is more sensitive to complex folding patterns of the brain surface (Lemaitre et al., 2012), and varies in association with age (Kochunov et al., 2005) and cognition (Liu et al., 2011).

The current study therefore aimed to 1) investigate whether the associations between a known predictor of cerebral health and integrity, namely physical activity, and brain structure can be detected with greater sensitivity using sulcal measures in place of or in addition to regional volumes using data from a large epidemiological cohort of older adults living in the community, and 2) assess whether the PA-related variability in brain measures, where present, is associated with cognitive function. It was predicted that greater levels of PA would be associated with deeper and narrower sulci, and with larger grey matter volumes in the adjoining areas. This effect was expected to be more prominent in the frontal lobe as this structure is known to be more sensitive to chronic disease and ageing processes and has previously been associated with PA (Colcombe et al., 2006). Moreover, it was predicted that where sulcal and/or volumetric measures were found to be related to PA, the regions identified would also be associated with cognitive function in domains known to be supported by these regions.