Research Byte: Executive functions are related to more than just the prefrontal strucutres--white matter matters

Neuroanatomical Substrates of Executive Functions: Beyond Prefrontal Structures

• Brianne M. Bettcher^{a, b, ,} ,
• Dan Mungas^c,
• Nihar Patel^a,
• Jonathan Elofson^a,
• Shubir Dutt^a,
• Matthew Wynn^a,
• Christa L. Watson^a,
• Melanie Stephens^a,
• Christine M. Walsh^a,
• Joel H. Kramer^a

• ^a University of California, San Francisco; Department of Neurology, Memory and Aging Center; San Francisco, CA
• ^b University of Colorado, Denver Anschutz School of Medicine; Departments of Neurosurgery and Neurology; Rocky Mountain Alzheimer’s Disease Center; Aurora, CO
• ^c University of California, Davis; Department of Neurology; Davis, CA

Received 6 August 2015, Revised 29 February 2016, Accepted 3 March 2016, Available online 3 March 2016

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Highlights

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Executive functions (EF) are not synonymous with ‘frontal’ tasks.

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Global atrophy was the only independent predictor of EF.

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Frontal volumes do not predict EF when statistically isolated from global atrophy.

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White matter metrics remain predictors of EF, independent of global atrophy.

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Abstract

Executive functions are often considered lynchpin “frontal lobe tasks”, despite accumulating evidence that a broad network of anterior and posterior brain structures supports them. Using a latent variable modeling approach, we assessed whether prefrontal grey matter volumes independently predict executive function performance when statistically differentiated from global atrophy and individual non-frontal lobar volume contributions. We further examined whether fronto-parietal white matter microstructure underlies and independently contributes to executive functions. We developed a latent variable model to decompose lobar grey matter volumes into a global grey matter factor and specific lobar volumes (i.e. prefrontal, parietal, temporal, occipital) that were independent of global grey matter. We then added mean fractional anisotropy (FA) for the superior longitudinal fasciculus (dorsal portion), corpus callosum, and cingulum bundle (dorsal portion) to models that included grey matter volumes related to cognitive variables in previous analyses. Results suggested that the 2-factor model (shifting/inhibition, updating/working memory) plus an information processing speed factor best explained our executive function data in a sample of 202 community dwelling older adults, and was selected as the base measurement model for further analyses. Global grey matter was related to the executive function and speed variables in all four lobar models, but independent contributions of the frontal lobes were not significant. In contrast, when assessing the effect of white matter microstructure, cingulum FA made significant independent contributions to all three executive function and speed variables and corpus callosum FA was independently related to shifting/inhibition and speed. Findings from the current study indicate that while prefrontal grey matter volumes are significantly associated with cognitive neuroscience measures of shifting/inhibition and working memory in healthy older adults, they do not independently predict executive function when statistically isolated from global atrophy and individual non-frontal lobar volume contributions. In contrast, better microstructure of fronto-parietal white matter, namely the corpus callosum and cingulum, continued to predict executive functions after accounting for global grey matter atrophy. These findings contribute to a growing literature suggesting that prefrontal contributions to executive functions cannot be viewed in isolation from more distributed grey and white matter effects in a healthy older adult cohort.

White matter matters! An oldie-but-goodie (OBG) post

White matter, in contrast to the grey squiggly mass (the cerebrum) that most people associate with the human brain, was for many years the research step-child to the cerebrum. That is no more. White matter, which has been called the brain's subway, super information system, or interstate highway communication system, now has a glass slipper. Research during the past decade has implicated white matter as performing the critical task of connecting and synchronizing different brain regions or networks so they can perform a wide variety of complex human cognitive or motor behaviors. The white matter system is considered the communication backbone system for the flow of information in the brain. Of particular interest (to me) is the parietal-frontal network, which is implicated as central to abstract human intelligence, fluid intelligence (Gf), working memory and attentional control (see prior posts re: the P-FIT model).

In a MindHub white paper I hypothesized that increasing white matter tract integrity may be a key mechanism behind the efficacy of the Interactive Metronome neuro-timing intervention (see figure below). I have gone as far as suggesting that the efficacy of many brain training/fitness programs may stem from a common domain-general effect--improving communication between and within various brain network(s) via more efficient white matter tract speed and communication. [Click on image to enlarge]

White matter integrity or dysfunction as been implicated in a wide variety of cognitive disorders or abilities, including cognitive control, math and intellectual giftedness, fluid intelligence or reasoning, processing speed, reading, decrease in cognitive functioning, meditation, working memory, vascular cognitive impairment, ADHD, autism, and cognitve and language maturation in infants. A sampling of recent white matter research article abstracts I have accumulated can be found by clicking here.
White matter matters!

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