cortex 49 (2013) 1771e1781 Available online at www.sciencedirect.com Journal homepage: www.elsevier.com/locate/cortex Research report The riddle of anosognosia: Does unawareness of hemiplegia involve a failure to update beliefs? Roland Vocat a, Arnaud Saj b and Patrik Vuilleumier a,b,* a Laboratory for Behavioral Neurology & Imaging of Cognition, Department of Neuroscience, Medical School, University of Geneva, Switzerland b Clinic of Neurology, University Hospital of Geneva, Geneva, Switzerland article info abstract Article history: Anosognosia for hemiplegia (AHP) is defined as a lack of awareness for motor incapacity Received 1 February 2012 after a brain lesion. The causes of AHP still remain poorly understood. Many associations Reviewed 10 May 2012 and dissociations with other deficits have been highlighted but no specific cognitive or Revised 30 August 2012 neurological impairment has been identified as a unique causative factor. We hypothe- Accepted 20 October 2012 sized that a failure to update beliefs about current state might be a crucial component of Action editor Giuseppe Vallar AHP. Here, we report results from a new test that are compatible with this view. We Published online 27 November 2012 examined anosognosic and nosognosic brain-damaged patients, as well as healthy con- trols, on a task where they had to guess a target word based on successive clues, with Keywords: increasing informative content. After each clue, participants had to propose a word solu- Anosognosia for hemiplegia tion and rated their confidence. Compared to other participants, anosognosic patients were AHP abnormally overconfident in their responses, even when information from the clues was Awareness insufficient. Furthermore, when presented with new clues incongruent with their previous Denial response, they often stuck to their former “false” beliefs instead of modifying them. This Hemiplegia impairment was unrelated to global deficits in reasoning or memory, and all patients Stroke eventually identified the correct solution of riddles after the last, fully informative, clue. These results suggest that a deficit in the generation and adjustment of beliefs may be a key factor contributing to the occurrence and persistence of anosognosia, when associated with concomitant losses in motor, proprioceptive, and/or attentional functions. Patients may remain unaware of their deficit partly because they cannot “update” their beliefs about current state. ª 2012 Elsevier Ltd. All rights reserved. 1. Introduction dysfunction. As initially described by Babinski (1914), the most common presentation is anosognosia for hemiplegia (AHP), Anosognosia is a striking neurological symptom that mani- where patients fail to recognize a severe motor deficit despite fests as unawareness and lack of concern of for their deficit direct confrontation during neurological examination. (hemiplegia, hemianopia, neglect, etc.) in brain-damaged pa- This lack of awareness can affect the motor deficit itself tients, and that cannot be explained by global cognitive (e.g., “I’m able to move my left arm”) but also its consequences * Corresponding author. Neurology & Imaging of Cognition, Department of Neuroscience & Clinic of Neurology, University Hospital (HUG), 24 rue Micheli-du-Crest, CH-1211 Geneva, Switzerland. E-mail address: [email protected] (P. Vuilleumier). 0010-9452/$ e see front matter ª 2012 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.cortex.2012.10.009 1772 cortex 49 (2013) 1771e1781 for a particular action (e.g., “I can open a bottle”) and/or its 1995; Gilmore et al., 1992; Lu et al., 2000, 1997), neuroana- general implications in everyday life (e.g., “I can go back to tomical studies have pointed to an involvement of many work”). The cognitive and neural mechanisms of this phe- different brain regions including the parietal lobe (Bisiach nomenon are poorly understood, and remain difficult to study et al., 1986; Heilman, 1991), insula (Karnath et al., 2005), pre- in a systematic way due the predominance of symptoms in motor, motor and sensory areas (Berti et al., 2005), thalamus acute stages and their heterogeneity (Vocat et al., 2010). Several (Starkstein et al., 1992), or more complex cortico-subcortical theoretical accounts of AHP have been proposed (Berti et al., circuits of motor control (Pia et al., 2004). Our own work 2005; Davies et al., 2005; Heilman, 1991; Levine et al., 1991; (Vocat et al., 2010) also highlighted a role for distributed le- Ramachandran, 1995; Weinstein and Kahn, 1955) but none of sions in areas associated with motor function, spatial atten- them appears sufficient to explain all the manifestations of tion, as well as interoceptive and affective functions, anosognosia, and the frequent dissociations with other disor- consistent with a multi-componential model of AHP. ders or between different domains of anosognosia itself (Vocat However, although the ABC model (Vuilleumier, 2004)or2- and Vuilleumier, 2010; Vuilleumier, 2000). Babinski (1914) factor delusional theory (Davies et al., 2005) made the hy- initially emphasized that AHP was often associated with pothesis that AHP might be critically linked to impairments in hemianesthesia and proprioceptive loss, possibly preventing the generation and adjustment of one’s beliefs in face of un- direct sensory experience of weakness, whereas Bisiach et al. certainty, no study has directly tested the ability of patients to (1986) insisted on a particular relation between AHP and check their belief accuracy and/or change their current be- spatial neglect which might disrupt conscious awareness of liefs. If anosognosics still rely on their past beliefs about their left hemibody. The discovery theory of Levine et al. (1991) health and are not able to modify them according to the new proposed that AHP could emerge due to a conjunction of condition (e.g., due to losses in sensory feedback, intentions, global cognitive impairment and impaired proprioception. A or bodily representations), they might indeed fail to correctly role for motor neglect was also highlighted as a possible acknowledge their current handicap. Here, we therefore causative factor by Heilman (1991), but related to a suppression designed a new neuropsychological test allowing us to of motor intention. Likewise, a deficit in comparator mecha- address this issue. Further, we aimed at using a task simple nisms that match the predicted movements (based on inten- and brief enough to be administered to patients at the bedside, tion) and the actual movement (based on sensory feedback) even in the acute stage. Our test required participants to make was also recently implicated (Bottini et al., 2010; Fotopoulou guesses in conditions where they should feel uncertain about et al., 2008; Frith et al., 2000). Finally, for Weinstein and Kahn their responses and could not be confident about their beliefs. (1955) and Turnbull et al. (2002), motivational or psychologi- Our main aim was to observe how patients with AHP could cal defense mechanisms could not be excluded. change their beliefs when confronted with incongruent in- More recent hypotheses (Davies et al., 2005; Vuilleumier, formation contradicting these beliefs. 2004) have suggested multiple causative factors. According to this view, AHP might emerge through various combinations of 2 (or more) deficits. Davies et al. (2005) proposed that AHP 2. Method could resemble delusions, requiring the presence of a first impairment that prompts delusional beliefs and a second 2.1. Population impairment that interferes with processes of belief evaluation which would otherwise allow rejecting the delusional belief. We tested 11 control participants (mean age 62.8 Æ 9.6, Similarly, Vuilleumier (2004) put forward a general “ABC 8 women, all right-handed), with no history of neurological or model” of anosognosia, where a combination of processes psychiatric diseases, and a group of 9 consecutive patients involving appreciation, belief, and check operations might with a first right hemispheric stroke and a full left hemiplegia. subserve awareness for motor losses, or cause anosognosia or The severity of AHP in these patients was measured using the denial when damaged in different ways in different patients. classical scale of Bisiach et al. (1986). Among them, 5 patients According to this view, the ability to modify one’s beliefs (mean age 56.4 Æ 16.8, 3 women, all right-handed) were able to together with the aptitude to monitor performance and out- give a good spontaneous description of their plegia (Bisiach comes in case of uncertainty might play a critical role in AHP, scale rating ¼ 0) and constituted the nosognosic group; in combination with other primary deficits in sensory, motor, whereas 4 other patients (mean age 60 Æ 10.2, 2 women, all and/or attentional functions (Venneri and Shanks, 2004). A right-handed) had clear and stable anosognosia for their recent elegant study (Jenkinson et al., 2009) also showed that hemiplegia (Bisiach score ¼ 3 in all of them) and were there- patients with AHP are impaired in reality monitoring pro- fore included in the anosognosic group. We did not test pa- cesses not strictly related to movement, but also extending to tients with intermediate Bisiach scores (ratings ¼ 1or2) visual perception. In keeping with multifactorial causes, a because it has been shown that measures of AHP may be recent prospective study (Vocat et al., 2010) showed that unreliable in these cases and represent only partial or fluc- different combinations of deficits and lesions have