Elsevier

NeuroImage

Volume 49, Issue 4, 15 February 2010, Pages 3358-3364
NeuroImage

Neuroanatomical correlates of cognitive self-appraisal in neurodegenerative disease

https://doi.org/10.1016/j.neuroimage.2009.11.041Get rights and content

Abstract

Self-appraisal is a critical cognitive function, which helps us to choose tasks based on an accurate assessment of our abilities. The neural mechanisms of self-appraisal are incompletely understood, although a growing body of literature suggests that several frontal and subcortical regions are important for self-related processing. Anosognosia, or lack of awareness of one's deficits, is common in neurodegenerative dementias, offering an important window onto the brain systems involved in self-appraisal. We examined the neuroanatomical basis of self-appraisal in a mixed group of 39 individuals, including 35 with cognitive impairment due to one of several probable neurodegenerative diseases, using voxel-based morphometry and an objective, neuropsychologically-based measure of self-appraisal accuracy. Self-appraisal accuracy was correlated with tissue content in the right ventromedial prefrontal cortex (vmPFC). We hypothesize that emotional/physiological processing carried out by vmPFC is an important factor mediating self-appraisal accuracy in dementia.

Introduction

Awareness of our own performance is a critical component of normal cognition that gives us the ability to recognize our limits and choose our activities accordingly. The neural basis self-awareness is incompletely understood, although a growing body of research suggests that several brain regions mediate functions relevant to self-appraisal, including medial prefrontal cortex, insula, anterior cingulate cortex, amygdala and other subcortical regions, and retrospenial cortex (Gusnard et al., 2001, Kelley et al., 2002, Northoff et al., 2006, Schmitz and Johnson, 2007).

Neurodegenerative diseases offer an important window into the mechanisms underlying self-awareness. Anosognosia, or lack of awareness of one's impairments, is very common in this setting (Mullen et al., 1996, Agnew and Morris, 1998, Zanetti et al., 1999). In contrast to classically-described anosognosia for left hemiplegia, which occurs in the setting of right frontoparietal lesions (McGlynn and Schacter, 1989) and appears to relate to insular damage (Karnath et al., 2005), neurodegenerative dementias impair insight into a variety of cognitive and emotional deficits, a form of anosognosia that may have a different neuroanatomical basis. Consistent with the literature supporting an important role for the frontal lobe in self-related processing, several previous studies have indicated that frontal lobe dysfunction, particularly on the right, strongly influences this loss of awareness of impairment (Reed et al., 1993, Starkstein et al., 1995, Mendez and Shapira, 2005, Vogel et al., 2005, Mimura and Yano, 2006, Salmon et al., 2006, Shibata et al., 2008), although the precise frontal regions associated with this deficit have not been determined. The prior studies examining the neural correlates of self-awareness in dementia measured awareness based on the discrepancy between subjective reports from patients and informants, whose own distress and potential cognitive impairments could be a potential source of inaccuracy (Clare, 2004). In this study, we examined the neuroanatomical correlates of self-appraisal accuracy using voxel-based morphometry and a measurement of self-appraisal that is dependent solely on objective neuropsychological testing, with demographically adjusted scores serving as the standard for comparing patient's self-appraisal ratings.

Section snippets

Participants

39 consecutively recruited individuals participated. To mitigate the potential contributions of disease-specific effects on self-appraisal, we included individuals with a range of diagnoses, representing a broad range of cognitive abilities, including two cognitively normal individuals, two cognitively normal patients with amyotrophic lateral sclerosis, two patients with mild cognitive impairment, nine patients with probable Alzheimer's disease (AD), ten with frontotemporal dementia (FTD), five

Group characteristics

Table 1 shows the demographic and cognitive data for the participants, grouped according to diagnosis as cognitively normal subjects (Controls and ALS), AD spectrum patients (MCI and AD), and FTD spectrum patients (FTD, SD, PNFA, CBD). Data are shown for the six tasks for which subjects predicted their performance, as well as for several tasks from our standard neuropsychological assessment battery tapping other domains, including verbal memory, language, visuospatial processing, calculations

Discussion

The chief finding in this study is that accuracy of self-appraisal for cognitive performance is correlated with gray matter content in the right vmPFC. Specifically, reduced vmPFC volume is associated with greater overestimation of cognitive performance. This relationship, which was identified using an objective, neuropsychologically-based assessment of self-appraisal, is independent of cognitive performance scores and diagnosis. The finding adds to a growing body of evidence supporting a role

Acknowledgments

This work was supported by the State of California DHS Alzheimer's Disease Research Center of California (ARCC) grant 06-55318, NIH grants, P50-AG023501, and P01-AG019724, grant number M01-RR00079 (UCSF General Clinical Research Center) and the Larry Hillblom Foundation. We wish to acknowledge Aaron Kaplan for his assistance in developing the visual aid for assessing self-appraisal in this study. We also gratefully acknowledge Bill Seeley and Arthur Shimamura for their generous advice on the

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