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The “self-awareness–anosognosia” paradox explained: How can one process be associated with activation of, and damage to, opposite sides of the brain? Alain Morin
Department of Psychology, Mount Royal University, Calgary, AB, Canada
ABSTRACT Healthy volunteers engaged in self-referential tasks such as reflecting on their personality traits exhibit mostly left lateralized brain activation, yet patients with lack of awareness of their deficit suffer from predominantly right hemisphere damage. How can the same basic process of self-awareness be associated with opposite sides of the brain? Anosognosia and self-awareness substantially differ on important dimensions and thus should not be equated. It is proposed that (1) anosognosia does not actually result from uniquely right hemisphere damage; (2) self-awareness and anosognosia do not constitute unitary concepts and encompass multiple other related processes, most likely associated with activity in distinct anatomical networks; and (3) impaired awareness of deficit is mostly caused by problems with self- monitoring, pre-/post-brain damage comparisons of performance, and episodic memory, and is more passive, unintentional, and about the body. Self-awareness produced by inviting participants to intentionally and actively think about more mental aspects of the self relies on judgements, inferential reasoning, imagination, and semantic memory. Consequently, the “self- awareness–anosognosia” paradox is only apparent. Furthermore, the claim that healthy self-awareness is located in the right hemisphere because anosognosia results from damage to this side of the brain must be fallacious.
ARTICLE HISTORY Received 12 December 2015; Accepted 28 March 2016
KEYWORDS Anosognosia; self-awareness; laterality; self-monitoring; judgements
Introduction
Several authors have claimed that areas within the right hemisphere of the brain generate self-awareness (Feinberg & Keenan, 2005; Gallup, 1998; Keenan, Gallup, & Falk, 2003; Keenan & Gorman, 2007; Keenan, Wheeler, Gallup, & Pascual-Leone, 2000). The argument is mainly based on the proposal that self-face recognition supposedly involves activation of prefrontal right hemispheric sites. This idea has been critically assessed as follows (Morin,
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CONTACT Alain Morin [email protected]
LATERALITY: ASYMMETRIES OF BODY, BRAIN AND COGNITION, 2017 VOL. 22, NO. 1, 105–119 http://dx.doi.org/10.1080/1357650X.2016.1173049
2003, 2007, 2010): (1) conceptually speaking, self-recognition cannot be equated with full-blown introspective self-awareness and (2) more recent self-face recognition studies implicate both hemispheres of the brain (Platek, Wathne, Tierney, & Thomson, 2008; Turk et al., 2002).
Another argument raised in favour of a right hemisphere bias for self-related processes relies on multiple neuropsychological reports which suggest that injury to the right hemisphere consistently produces disturbances of the self (Feinberg, 2011). The most frequently noted self-disorder is anosognosia— the unawareness that one exhibits objective deficits produced by brain damage (Pia et al., 2014). In simple terms, the idea is that (1) anosognosia is mostly linked to right hemispheric damage, (2) anosognosia represents a deficit of self-awareness, and (3) intact self-awareness most likely is the result of right hemisphere activity—perhaps a less extreme version is that the right hemisphere thus importantly contributes to the construction of self-awareness.
This reasoning creates a paradox that has not yet been addressed in the neurocognitive literature, hereafter called the “self-awareness–anosognosia” paradox. Healthy participants engaged in self-referential tasks such as reflect- ing on their personality traits, past memories, future imagined events, or emotions exhibit mostly left lateralized brain activation (Denny, Kober, Wager, & Ochsner, 2012), yet patients with lack of awareness of their deficit suffer from predominantly right hemisphere damage. How can self-awareness be associated with left hemisphere activation for self-referential tasks and with the right hemisphere when it is compromised? In what follows I define anosognosia and self-awareness, review their respective lateralization biases, and offer a tentative solution to the “self-awareness–anosognosia” paradox. This leads to a critical examination of the aforementioned reasoning linking healthy self-awareness with the right hemisphere.
Anosognosia: overview and anatomical location
Overview
Anosognosia refers to a more or less extensive lack of awareness of several forms of sensory, motor, perceptual, cognitive, and/or emotional disturbances following brain damage caused by a stroke, traumatic brain injury, or multiple neurodegenerative conditions such as Alzheimer’s disease and dementia (Rosen, 2011; Starkstein, Jorge, & Robinson, 2010). It has been shown to be associated with a wide array of diagnoses, including hemiplegia, hemianaesthe- sia, hemineglect, cortical blindness, aphasia, executive dysfunctions, and amnesia (Godefroy & Stuss, 2007). Thus, anosognosia does not represent a unitary phenomenon. Specifically, it is very heterogeneous across conditions, with different neural correlates and presentations for anosognosia for hemiple- gia, dementia, traumatic brain injury, and so on. To illustrate, anosognosia for
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hemiplegia is the denial of the contralesional motor deficits that follow brain damage. According to Pia, Neppi-Modona, Ricci, and Berti (2004), it most fre- quently occurs in association with unilateral right-sided or bilateral lesions of frontal, parietal, and temporal cortical structures, as well as subcortical lesions. In contrast, anosognosia for dementia involves both cognitive unaware- ness (problems with memory, spatial and temporal orientation, calculation, abstract reasoning, and praxis) and behavioural unawareness (irritability, selfish- ness, inappropriate emotional display, and instinctive disinhibition) (Starkstein, Sabe, Chemerinski, Jason, & Leiguarda, 1996). Anosognosia in Alzheimer’s disease is mostly linked to frontal lobes dysfunction (Pia & Conway, 2008).
Patients suffering from anosognosia may be oblivious of one deficit while acknowledging another one (Starkstein et al., 2010). The unawareness of dys- function can be the partial result of psychological denial for self-protective purposes, but it is widely recognized that in most cases, anosognosia is not psychologically orchestrated given the flat affect state (i.e., indifference) that characterizes patients—ruling out emotional distress caused by the con- dition as a underlying self-escape motive (Peskine & Azouvi, 2007). Several assessment tools exist to identify and quantify anosognosia, among which are interviews, self-rating questionnaires, and match (or lack thereof) between self-/other ratings of patients’ performance, behaviour, and person- ality traits (Cocchini, Beschin, & Della Sala, 2012). Morris and Mograbi (2013) explored influential explanatory models of anosognosia in Alzheimer’s disease (potentially applicable to anosognosia in general) and concluded that the most convincing view entails a loss of mnemonic ability in which knowledge about self-ability is degraded, leading to outdated self-knowledge of current motor performance, mental abilities, sensory experiences, social behaviour, and so on. Anosognosia is not a trivial condition as it renders the patient uninterested in his or her condition and unmotivated to actively participate in the rehabilitation process, therefore decreasing the likelihood of recovery (Peskine & Azouvi, 2007).
Right hemisphere bias
Evidence for a right hemisphere bias in anosognosia seems substantial. This question has been extensively examined elsewhere, thus I will summarize this point here. Multiple research papers report that anosognosia results from right hemisphere anaesthesia (Breier et al., 1995; Heilman & Harciarek, 2009) and lesions (Bisiach, Vallar, Perani, Papagno, & Berti, 1986; Long, Rager, & Adams, 2014; Pia et al., 2014; Rosen, 2011; Starkstein, Fedoroff, Price, Leiguarda, & Robinson, 1992; Vossel, Weiss, Eschenbeck, & Fink, 2013). Martins, Caeiro, and Ferro (2007) exclusively discuss anosognosia under their section on right hemispheric cognitive and neuropsychiatric syndromes. One part of Godefroy and Bogousslavsky’s book (2007) on strokes presents
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five chapters on hemineglect under the heading right hemisphere syndromes. A search for mentions to right hemisphere damage/left-sided awareness of deficit versus left hemisphere damage/right-sided unawareness in Prigatano’s (2009) historical review of anosognosia reveals 11 mentions of the former and 2 of the latter. Orfei, Caltagirone, and Spalletta (2009) reviewed 20 indepen- dent studies of large groups of patients suffering from anosognosia following a stroke and found that 12 studies reported left- and right-sided lesions, 7 reported uniquely right-sided lesions, and 1 did not specify laterality; not a single report out of the 20 noted uniquely left-sided damage.
Self-awareness: overview and anatomic location
Overview
Although consciousness usually refers to the processing of information coming from the external environment (Natsoulas, 1996), with wakefulness/responsive- ness being a prerequisite (Merker, 2007), self-awareness constitutes the ability to become the object of one’s own attention (Duval &Wicklund, 1972) and involves actively identifying, processing, and storing information from the internal environment—the self (Morin, 2006). It is crucial to acknowledge that two types of self-awareness have been identified: self-reflection and self-rumination (Trapnell & Campbell, 1999). Self-reflection, including mindfulness, underlies a healthy, genuine curiosity about the self and leads to heightened self-regulation and overall well-being, whereas self-rumination (self-absorption) refers to an unhealthy excessive and redundant self-focus associated with depression and social anxiety (Joireman, 2004; Joireman, Parrott, & Hammaersla, 2002). Various measures and manipulations of self-awareness exist, among which are exposure to self-focusing stimuli (Duval & Wicklund, 1972), self-report questionnaires (Fenigstein, Scheier, & Buss, 1975; Govern & Marsch, 2001), first-person singular pronouns use (Wegner & Giuliano, 1980), and self-recognition (Gallup, 1968).
Left hemisphere bias
In sharp contrast with the right hemispheric bias for lesions observed in patients suffering from anosognosia (especially hemiplegia), several self- referential tasks completed by healthy patients tend to recruit a left lateralized brain circuit (Bergström, Vogelsang, Benoit, & Simons, 2015; D’Argembeau et al., 2014; Herwig, Kaffenberger, Schell, Jäncke, & Brühl, 2012; Lalanne, Grol- leau, & Piolino, 2010; van der Meer et al., 2013; Munevar et al., 2014; Shad et al., 2012)—hence the apparent “self-awareness–anosognosia” paradox. Typical tasks used in this context are summarized in Table 1 (Morin, 2013). One poss- ible—yet speculative—reason for this left hemisphere asymmetry may be that self-reflection often recruits inner speech (Morin, 2005, 2015), which is linked to left inferior frontal gyrus activation (Morin & Hamper, 2012).
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Cortical midline structures also appear to be particularly important for self- awareness (D’Argembeau et al., 2008; Northoff, 2014; Ries et al., 2007; Summerfield, Hassabis, & Maguire, 2009). Moran, Kelley, and Heatherton (2013) suggest that cortical midline structures are specialized for representing any type of social information, including the self; they are also responsible for the direction of our thought processes on a moment-to-moment basis and constitute a hub integrating information from various neural processing systems into a “conscious workspace” (Baars, 2002). Recent research also suggests that ventral medial prefrontal cortex gets more activated as stimuli presented to participants gain more personal relevance (self-related- ness), whereas dorsal medial prefrontal cortex gets more activated when stimuli represent other persons (Abraham, 2013; Molnar-Szakacs & Uddin, 2013; Moran, Heatherton, & Kelley, 2009).
Patterns of brain activity differ across various self-domains. Not all self- referential processes show a left hemisphere bias: in particular, agency tasks tend to recruit right-sided sites (Farrer & Frith, 2002), whereas thinking about one’s personality traits, past, future, intentions, and emotions rely more on left hemisphere activation (Morin, 2011). Molnar-Szakacs and Uddin (2013) propose that self-processes can be divided into physical and psychological. Reflecting on aspects of the physical self (e.g., one’s face in self-recognition tasks) is associated with activity in the mirror neuron system mostly located in the right hemisphere, whereas reflecting on one’s mental states and more abstract self-characteristics (e.g., personality traits) is linked to activation of the medial prefrontal cortex. In a meta-analysis reviewing 107 published neuroimaging studies of self-referential activity, Denny et al. (2012) noted that: “… self-related judgments were associated with almost entirely left-lateralized activity, including left ventro prefrontal cortex, left anterior and mid-insula, and dorsal caudate… ” (p. 1748).
The “self-awareness–anosognosia” paradox explained
As mentioned earlier, the above presentation raises the following dilemma: How can one process be associated with activation of, and damage to, oppo- site sides of the brain? In other words: How can the neuropsychology
Table 1. Typical self-tasks across self-domains. Self-domain Self-task
Agency Driving circle along T-shaped path either by oneself or experimenter Self-recognition Judging if face is self or other Personality traits Judging if various traits, activities, and emotions are self-descriptive Autobiography Recalling autobiographical memories in response to visual cues Emotions Evaluating one’s emotional responses to visual cues First-person perspective Contemplation of information from first- versus third-person perspective Various (e.g., prospection) Pre-experiencing future personal events in response to visual cues
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literature propose that, based on anosognosia, self-awareness is the result of right hemisphere activity while the cognitive neuroscience literature suggests that self-referential processes activate mostly left hemispheric sites?
One first possibility is that anosognosia does not actually result from uniquely right hemisphere damage. The apparent right hemisphere bias noted earlier particularly applies to hemiplegia. In traumatic brain injury patients for instance, an functional magnetic resonance imagery self-appraisal task pertaining to one’s traits and abilities produced activation at midline pre- frontal and retrosplenial cortices, as well as in the anterior cingulate, precuneus, and right temporal pole (Schmitz, Rowley, Kawahara, & Johnson, 2006). This team further suggested that patients’ post-injury level of self-referential insight was related to a network inclusive of themedial and right dorsal prefron- tal cortex. Impaired self-evaluation in Alzheimer’s disease is associated with a decrease in brain metabolism in orbital prefrontal cortex and in medial temporal structures (Salmon et al., 2006). Also, Cocchini, Cameron, Beschin, and Fotopoulou (2009) have suggested that (1) the estimation of right hemisphere implication in anosognosia may have been inflated because of the frequent exclusion of left hemisphere damaged patients (who are more difficult to test given their frequent language problems) and (2) some left hemi- sphere lesions do lead to anosognosia. To illustrate, anosognosia for motor impairment following left brain damage has been observed (Cocchini et al., 2009). Cohen, Rémy, Leroy, Gény, and Degos (1991) report the case of a patient with asomatognosia and anosognosia for right hemiplegia caused by a left hemisphere lesion.
A second possible reason why there is no real “self-awareness–anosogno- sia” paradox is that self-awareness constitutes much more than just attention directed towards the self. That is, like anosognosia, self-awareness does not constitute a unitary concept and encompasses multiple other related pro- cesses as briefly described in Table 2; Figure 1 depicts the postulated relation- ship between some of these self-related processes (both from Morin & Clements, 2015). More specifically, self-awareness involves—and leads to— self-description, self-evaluation, self-recognition, self-rumination, self-regu- lation, self-esteem, and so on, each of these most likely being associated with activity in distinct anatomical networks. As a result, clearly, self-aware- ness and anosognosia differ substantially and thus must not be equated.
Let me further elaborate this point as follows. Although anosognosia and self-awareness share some common features (e.g., both obviously deal with information about the self), they nonetheless substantially differ on other important dimensions. I submit that two of these differences between ano- sognosia and self-awareness are the (1) underlying mental processes and (2) self-knowledge content involved. Table 3 schematically presents these differences, as well as others discussed below.
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One first proposed difference pertains to the mental operations required by healthy participants to complete self-tasks and those lacking in patients with anosognosia. In essence, anosognosia represents an impairment of anatomo-functionally discrete monitoring systems (Moro, Pernigo, Zapparoli, Cordioli, & Aglioti, 2011; Vallar & Ronchi, 2006). Patients unaware of deficits have difficulties (1) consolidating information about current task failures (e. g., “last Sunday I was unable to tie my shows using my left hand”), (2) remem- bering more remote personal episodes with such tasks (episodic memory deficit, e.g., “two years ago I did not have this problem”), and thus (3) compar- ing (monitoring, appraising) differences in performance (and sensory experi- ences, social, cognitive functioning, etc.) between two distinct time periods: pre- and post-brain damage periods (Morris & Mograbi, 2013). On the other
Table 2. Various processes related to self-awareness. Process Reference
Bodily awareness Kyselo (2014) Thinking about all possible private (internal) and public (visible) self-aspects
Fenigstein (1987)
Thinking about one’s past (autobiography) and future (prospection)
Szpunar (2010)
Self-description Marsh (1994) Self-knowledge Wilson (2009) Self-concept formation L’Ecuyer (1978) Self-evaluation Higgins (1987) Self-esteem Rosenberg (1965) Sense of agency Farrer and Frith (2002) Mindfulness Carlson (2013) Self-regulation Baumeister and Vohs (2003) Self-efficacy Bandura (1977) Theory-of-mind Dimaggio, Lysaker, Carcione, Nicolo, and
Semerari (2008)
Figure 1. Postulated relations between various self-related processes. Note: SA = self- awareness; IS = inner speech.
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hand, self-awareness tasks typically used during brain-imaging studies unli- kely rely on the aforementioned processes of self-monitoring and episodic memory. Rather, healthy participants in self-reflection studies are primarily asked to make judgements about hand movements (agency), faces (self- recognition), traits, emotions, intentions, preferences, and so on. These judge- ments are based on inferential reasoning because they involve a certain degree of uncertainty (Legrand & Ruby, 2009): Does this personality trait apply to me? Is this my face? Did I move my hand? Trait judgements appear to depend on semantic, as opposed to episodic, memory.1 Some other self-reflection tasks invite volunteers to imagine future personal events (prospection), recall past personal experiences (autobiography), or per- ceive information (e.g., scenes, emotions) from a first versus third person per- spective. Again, the cognitive processes underlying awareness of deficits (lacking in anosognosia) and self-reflection seem to fundamentally differ.
Table 3. Main postulated differences between anosognosia and self-awareness. Anosognosia Self-awareness
Underlying mental processes – Self-monitoring, appraisal – Thinking about behavioural/sensory/cognitive differences between pre- and post-damage time periods
– Remembering personal experiences of deficit(s) post-damage for pre- damage comparison purposes
– Episodic memory
– Judgements – Imagination – Inferential reasoning – Semantic memory
Self-knowledge content – Performance (motor, social, intellectual, etc.) – Sensory experiences – Deficits – Body
– Traits – Preferences – Intentions – Emotions – Self-initiated behaviour (agency)
– Face – Past personal experiences – Future imagined personal experiences
Mostly about body Mostly about mental – Lack of awareness of deficit – Self-knowledge deficit – Awareness of multiple self-
aspects – Self-knowledge access
Passive: Constant lack of deficit awareness in background manifests itself during interviews about performance
Active: Ongoing self- referential task
Unintentional Intentional
1 Such personality trait judgements have been shown to remain intact and accurate in patients suffering from episodic memory problems (Klein, Cosmides, & Costabile, 2003). More precisely, evidence suggests that people first develop knowledge of personality traits by evoking specific past examples of beha- viours (episodic memory, e.g., “I was on time for class today”) and gradually translate these into more abstract self-representations that become semantic in nature (e.g., “I am punctual”). Thus, access to self-knowledge of traits via semantic memory remains intact when episodic memory is compromised.
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Types of self-knowledge involved in impaired awareness of deficits and healthy self-awareness also seem widely distinct. What patients with anosog- nosia are mostly asked to think about relates to motor performance deficits and bodily sensory experiences, whereas as seen above, healthy individuals working on self-referential tasks reflect on their traits, preferences, intentions, emotions, self-initiated behaviour (agency), facial features, past personal experiences, and future imagined personal experiences.
Yet another difference is that anosognosia, with the exception of lack of awareness of cognitive and emotional deficits, tends to be more about the body (e.g., hemiplegia, hemianaesthesia, hemineglect), whereas self-aware- ness (with the exception of facial self-recognition and agency) entails more psychological abstract self-aspects such as traits, intentions, and emotions (Morin & Hamper, 2012).
Finally, I wish to mention three additional potential differences between anosognosia in brain-injured patients and self-reflection in healthy individ- uals: (1) anosognosia underlies a lack of awareness (of deficit), whereas self- awareness is about access to self-information; (2) anosognosia seems to rep- resent a more passive process where the patient lacks awareness of deficit until it gets objectified during clinical interviews about current versus past performance, whereas self-awareness tasks are more ongoing—active; and (3) related to this last point, self-reflective processes seem intentional in the sense that participants are invited to willfully engage in self-tasks, which is less the case in anosognosia patients.
Conclusion
In light of the differences between anosognosia and self-awareness discussed above, it is safe to conclude that the main reason that both have been associ- ated with opposite sides of the brain—an apparent paradox—is because they are not identical. Once the definitions are made more precise, the paradox dis- appears. Anatomo-functional dissociations in anosognosia can be considered as one of its main characteristics. For example, anosognosia for hemiplegia can be dissociated from other denials (e.g., anosognosia for neglect) as well as from other components within the same domain (e.g., motor intention and awareness of the consequences of a willed action). This casts doubts on the idea of unitary self-awareness in intact brain functioning—hemispheric dominance included. Also, while anosognosia constitutes a lack of awareness of deficits following brain damage, self-awareness entails actively identifying, processing, and storing information about the self in a healthy brain. Further- more, lack of awareness of deficit is generally caused by problems with self- monitoring, pre-/post-brain damage comparisons of performance, and episo- dic memory, and is more passive, unintentional, and about the body. Self- awareness produced by inviting participants to intentionally and actively
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think about more mental aspects of the self relies on judgements, inferential reasoning, imagination, and semantic memory. If this analysis is correct, then it follows that any claim to the effect that healthy self-awareness is located in the right hemisphere because anosognosia and other self-disturbances result from damage to this side of the brain (Feinberg, 2011; Feinberg & Keenan, 2005; Keenan & Gorman, 2007) must be fallacious.
Acknowledgements
I would like to thank Daniel Mograbi, Famira Racy, Hanaa Elmoghrabi, Christina Camp- bell, and an anonymous reviewer for their constructive comments made on previous versions of this paper.
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- Abstract
- Introduction
- Anosognosia: overview and anatomical location
- Overview
- Right hemisphere bias
- Self-awareness: overview and anatomic location
- Overview
- Left hemisphere bias
- The “self-awareness–anosognosia” paradox explained
- Conclusion
- Acknowledgements
- References