Review articleSelf-awareness and the medial temporal lobe in neurodegenerative diseases
Introduction
Awareness can be defined as “a reasonable or realistic perception or appraisal of one’s situation, functioning or performance, or of the resulting implications, expressed explicitly or implicitly” (Clare et al., 2011). Accurate self-awareness is essential for optimal daily life activities, as it allows adapting individual behaviour to different situations according to one’s actual abilities. Accurate self-awareness thus prevents from risky or withdrawal behaviour.
Impaired self-awareness may have significant adverse effects. For instance, overestimation of one’s driving or postural abilities increases the risk of driving or fall accident (Morone et al., 2014, Horrey et al., 2015), and overestimation of one’s cognitive abilities may negatively impact numerous daily life activities such as managing finances or shopping (Hoofien et al., 2004); likewise, inaccurate estimation of one’s social skills may affect social communication. Conversely, underestimation of these same abilities may lead to a loss of autonomy and social isolation. However, overestimation is more common than underestimation of one’s abilities (e.g. Michon et al., 1994, Okonkwo et al., 2008). Unawareness of deficits can be detrimental to the rehabilitation of brain damage. It also affects the patient’s family and friends’ quality of life, namely by increasing the caregivers’ burden (Rymer et al., 2002). Although impaired self-awareness should thus be considered as a symptom of great importance, it is often neglected, mainly because of the lack of knowledge of its pathophysiology, treatment and prevention.
Impaired self-awareness has been reported in a number of neurological and neuropsychiatric disorders (e.g. stroke, neurodegenerative diseases, traumatic brain injury, schizophrenia), and in various domains (e.g. sensori-motor, cognitive, socio-emotional, and daily life activities). This clearly demonstrates that there is no “awareness centre” in the brain, but rather suggests that self-awareness implies several areas likely organized in specific networks.
Attempts to unravel the brain networks involved in impaired self-awareness have been the focus of a number of studies. The medial prefrontal cortex is the most constantly identified region within this network. Other cortical and sub-cortical areas have been implicated. However, their role in self-awareness remains obscure (see Northoff et al., 2006 for meta-analysis). Among them, the medial temporal lobe (MTL) structures stand out, namely the hippocampus, amygdala, and surrounding cortices, i.e. the temporopolar, entorhinal, perirhinal and posterior parahippocampal cortices.
This review aims at providing an in depth analysis of the putative role of MTL in impaired self-awareness in neurodegenerative diseases, because this symptom is common in these conditions that are often associated with MTL damage albeit to varying degrees. Moreover, involvement of MTL in impaired self-awareness has never been explored specifically. Thus, we will focus on five of such neurodegenerative diseases: Alzheimer’s disease (AD), frontotemporal dementia (FTD), Parkinson’s disease (PD), Huntington’s disease (HD), and amyotrophic lateral sclerosis (ALS). Mild cognitive impairment (MCI) has also been included in the review because many symptoms are shared and quite a few individuals will convert to AD.
Section snippets
Methodological assessment procedures
The most frequently used method of assessing self-awareness is to compare the participant’s judgments about its own abilities and behaviour with parallel ratings made by an informant (e.g. spouse and caregiver). Several validated questionnaires and standardized procedures have been developed (eg, Wilson et al., 1989, Clare et al., 2002, Starkstein et al., 2006, Bramham et al., 2009). This method, however, lacks direct measurement of performance, and a range of psychological and social factors
Medial temporal lobe and awareness in neurodegenerative diseases
Brain networks of self-awareness in neurodegenerative diseases were mainly investigated by assessing the brain correlates of self-awareness (using structural MRI or metabolic FDG-PET imaging for instance) or in participants performing a self-awareness task (e.g. fMRI). Up to date, there is only one postmortem anatomical study (Marshall et al., 2004), and it provided little significant information due to various methodological limitations (e.g. only four areas investigated, etc.).
Structural or
Functional interpretation of neuroimaging findings on self-awareness in neurodegenerative diseases
Three main salient points emerge from the review of the above neuroimaging studies. First, despite the numerous differences in the methodological procedure used in the different studies (e.g. population, awareness assessment, imaging techniques, statistical analyses), the MTL structures that show structural or functional changes in patients who overestimate their abilities are essentially consistent from one study to the other, especially when analysed by awareness domain. Second, structural or
Future directions and conclusion
In view of the present review, there is a need for further neuroimaging investigations focusing on MTL in the various domains of self-awareness and in the different neurodegenerative diseases. In addition, the search for other brain centres involved in self-awareness, as the present endeavour regarding the role played by the MTL, is a potentially fruitful avenue for future studies designed to advance in the knowledge of the biological basis of self-awareness. Special attention should in
Acknowledgements
The authors wish to thank the personnel of the Human Neuroanatomy Laboratory of the University of Castilla-La Mancha as well as E Monfardini (INSERM U1028, CNRS UMR5292) for their valuable help in neuroanatomy and neuroimaging analyses. Supported by grants BFU-06-12964 and BFU09-14705 from MINECO, Spain.
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