Hippocampal atrophy and intrinsic brain network dysfunction relate to alterations in mind wandering in neurodegeneration

Abstract

Mind wandering represents the human capacity for internally focused thought and relies upon the brain's default network and its interactions with attentional networks. Studies have characterized mind wandering in healthy people, yet there is limited understanding of how this capacity is affected in clinical populations. This paper used a validated thought-sampling task to probe mind wandering capacity in two neurodegenerative disorders: behavioral variant frontotemporal dementia [(bvFTD); n = 35] and Alzheimer's disease [(AD); n = 24], compared with older controls (n = 37). These patient groups were selected due to canonical structural and functional changes across sites of the default and frontoparietal networks and well-defined impairments in cognitive processes that support mind wandering. Relative to the controls, bvFTD patients displayed significantly reduced mind wandering capacity, offset by a significant increase in stimulus-bound thought. In contrast, AD patients demonstrated comparable levels of mind wandering to controls, in the context of a relatively subtle shift toward stimulus-/task-related forms of thought. In the patient groups, mind wandering was associated with gray matter integrity in the hippocampus/parahippocampus, striatum, insula, and orbitofrontal cortex. Resting-state functional connectivity revealed associations between mind wandering capacity and connectivity within and between regions of the frontoparietal and default networks with distinct patterns evident in patients vs. controls. These findings support a relationship between altered mind wandering capacity in neurodegenerative disorders and structural and functional integrity of the default and frontoparietal networks. This paper highlights a dimension of cognitive dysfunction not well documented in neurodegenerative disorders and validates current models of mind wandering in a clinical population.

Keywords: Alzheimer’s disease; behavioral variant frontotemporal dementia; default mode network; hippocampus; mind wandering.

Fig. 1.

(A) Overall proportion of mind wandering scores across participant groups. Percentage responses across the mind wandering continuum. The asterisks show the main results of group differences at Level 1 and Level 4. Level 1 responses represent stimulus-bound thoughts; Level 4 responses denote fully fledged instances of mind wandering. (B) Average mind wandering index scores. Mind wandering index (i.e., percentage difference in Level 4 minus Level 1 responses). Higher scores reflect an increased propensity to engage in mind wandering as opposed to stimulus-bound thought with lower scores reflecting a tendency toward stimulus-bound thought. *P < 0.05; **P < 0.01; ***P < 0.001.

Fig. 2.

The regions of gray matter intensity that covaried with the mind wandering index in bvFTD and AD patients combined. Significant clusters were identified in the striatum (including caudate, putamen, and nucleus accumbens) and the anterior–mid thalamus, extending to the left subcallosal, medial/lateral orbitofrontal and anterior insular cortices; the left hippocampus, parahippocampal gyrus, and the left posterior insular cortex. Results are familywise error (FWE) corrected at P < 0.01; significant clusters identified using threshold free cluster enhancement.

Fig. 3.

Seed regions where connectivity was associated with a tendency to mind wander within the participant groups. Connections show where the mind wandering index was significantly correlated with connectivity such that a tendency to mind wander on the task (as opposed to stimulus-bound thought) was either positively (red lines) or negatively (gray lines) associated with connectivity. The color of regions of interest (ROIs) correspond to the networks the regions are taken from: DN, default network; FPN, frontoparietal network; HC, hippocampus. The results are false discovery rate (FDR) corrected at q < 0.05. amPFC, anteromedial prefrontal cortex; dlPFC, dorsolateral prefrontal cortex; HF, hippocampal formation; PCC, posterior cingulate cortex; postHC, posterior hippocampus; vmPFC, ventromedial prefrontal cortex. Left view = left side of brain; Right view = right side of brain.