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Special issue: Review
Somatoparaphrenia: Evolving theories and concepts Todd E. Feinberg a,* and Annalena Venneri b a Departments of Psychiatry and Neurology, Icahn School of Medicine at Mount Sinai and the Yarmon Neurobehavior and Alzheimer's Disease Center, Mount Sinai Beth Israel, New York, NY, USA b Department of Neuroscience, University of Sheffield, UK and IRCCS San Camillo Foundation Hospital, Venice, Italy
article info
abstract
Article history:
Somatoparaphrenia, a syndrome that involves at a minimum unawareness of ownership
Received 1 December 2013
of a body part, in addition involves productive features including delusional misidentifi-
Reviewed 22 January 2014
cation and confabulation. In this review we describe some of the clinical and neuroana-
Revised 26 February 2014
tomical features of somatoparaphrenia highlighting its delusional and confabulatory
Accepted 1 July 2014
aspects. Possible theoretical frameworks are reviewed taking into account cognitive, psy-
Published online 22 July 2014
chodynamic, and philosophical views. We suggest that future studies should approach this syndrome through investigations of structural and functional connectivity and focus on
Keywords:
the possible interplay between alterations in major functional networks of the brain, such
Somatoparaphrenia
as the default mode and salience networks, but also take into account motivational
Asomatognosia
variables.
Delusional misidentification
© 2014 Elsevier Ltd. All rights reserved.
Confabulation Self-boundaries
1.
Asomatognosia and somatoparaphrenia
After Babinski first coined the term “anosognosia” (1914, 1918), Gerstmann (1942) suggested that there were three “indirect disorders of the body scheme” that were characterized by an abnormal experience of, behavior toward, or verbal statements about a function of or part of the body. In all three of these conditions, the most common clinical presentation involves an abnormal attitude toward the left arm in the setting of right hemisphere damage, or deficit of awareness for left hemiplegia, hemisensory deficits and hemispatial neglect
(Critchley, 1953; 1955; Feinberg, Haber, & Leeds, 1990; Feinberg, Venneri, Simone, Fan, & Northoff, 2010; Feinberg, 2009; Gerstmann, 1942; Halligan, Marshall, & Wade, 1995; Vallar & Ronchi, 2009). The first of these was anosognosia itself (lack of knowledge of disease) referred to by Gerstmann as “cases of imperception of disease or defect in function” (1942, p. 909). Second were cases of “imperception of the defective parts or side of the body, with forgetting of their existence or non recognition of their possession” (1942, p. 909). It was this condition that Critchley (1953) later called asomatognosia (“lack of knowledge of the body”). The third syndrome Gerstmann (1942) called
* Corresponding author. Yarmon Neurobehavior and Alzheimer's Disease Center, Mount Sinai Beth Israel, 1st Avenue at 16th Street, New York, NY 10003, USA. E-mail address: [email protected] (T.E. Feinberg). http://dx.doi.org/10.1016/j.cortex.2014.07.004 0010-9452/© 2014 Elsevier Ltd. All rights reserved.
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somatoparaphrenia, which was essentially a variant of asomatognosia involving delusional beliefs about the contralesional side of the body: “For the condition predominating in cases of the third group, I believe the designation somatoparaphrenia to be suitable, since it takes account of the fact that in the negative state of experience of absence of a certain part or area of the body, induced by disease, positive psychopathological phenomena in the sphere of the body scheme are apt to occur” (Gerstmann, 1942, p. 909). According to Gerstmann (1942), in somatoparaphrenia, the experience of absence of the affected limb is associated with “illusional, confabulatory or delusional ideas of a peculiar nature” (p. 909). Critchley (1955) later added, among the more common features of somatoparaphrenia, personification of the paralyzed limbs in which the contralesional limbs are conferred a separate identity and may be said to belong to a relative, a child or a pet (Critchley, 1953, 1955; 1974; Feinberg, 2009; Feinberg et al., 2010), and misoplegia (Critchley, 1974; Loetscher, Regard, & Brugger, 2006; Pearce, 2007) in which the limb is hated, abused, or physically attacked (Table 1; See Vallar and Ronchi (2009) for a comprehensive review of some additional descriptive distinctions). This review will focus mainly on those cases and group studies in which somatoparaphrenic delusions were the most prominent symptoms, and were accompanied by confabulations. A description of a sample of these cases is shown in Table 1.
2.
The neuroanatomy of somatoparaphrenia
In the first large study of the neuroanatomy of asomatognosia, Feinberg et al. (1990) compared 12 patients with right hemisphere strokes, asomatognosia, and hemispatial neglect with 4 patients with neglect but without asomatognosia. For the purposes of this study, any patient who verbally denied ownership of the limb was deemed to display asomatognosia whether or not delusions or confabulations were present. Thus, these cases included both Gerstmann's second type (Critchley's asomatognosia), and Gerstmann's third type (somatoparaphrenia). This study reported damage to the supramarginal gyrus in the inferior parietal lobule and its subcortical connections within the posterior corona radiata to be the most common lesions in these cases and were significantly more common than in a control group of patients with right hemisphere lesions and hemispatial neglect but without asomatognosia of any form. In the next group study, Baier and Karnath (2008) studied “disturbed sensation of limb ownership” (DSO) in a group of 12 right hemisphere damaged patients with anosognosia for hemiplegia. DSO designated a fairly broad group of symptoms and included cases of somatoparaphrenia, misoplegia, and personification of the limb, but also cases of anosodiaphoria, kinesthetic hallucinations, and supernumerary phantom limb, the latter symptoms not traditionally designated within the somatoparaphrenia syndrome. In this broad group they found that 11/12 (91.7%) patients demonstrated DSO, and within this group damage to right posterior insula was the
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critical region. However, in that study cases of somatoparaphrenia were not independently analyzed from cases of anosodiaphoria, kinesthetic hallucinations, and supernumerary phantom limb. The Feinberg et al. (1990) study did not distinguish between patients with asomatognosia and those with somatoparaphrenia, the latter specifically including cases with confabulation, delusions, delusional misidentifications, or personifications of the limb. These two syndromes have significant clinical distinctions and to see whether these differences were associated with significant neuroanatomical differences, Feinberg et al. (2010) compared cases with simple asomatognosia (asomatognosia only group) who showed unelaborated errors regarding the ownership of the limb, to cases with somatoparaphrenia who had asomatognosia plus extensive delusions, misidentifications, and confabulations regarding the limb and controls with hemispatial neglect but neither asomatognosia or somatoparaphrenia. In this study we found that all patients with asomatognosia only or somatoparaphrenia, as well as controls, had significant temporoparietal involvement or, less commonly, damage to other structures such as the insula that have been implicated in the feeling of ownership of the limb (Baier & Karnath, 2008). Thus, involvement of posterior temporoparietal regions was critical to the establishment of both asomatognosia and somatoparaphrenia. However, patients with somatoparaphrenia had the overall largest lesions and significantly more right medial frontal involvement than patients with simple asomatognosia. Furthermore, while patients with asomatognosia only had more medial frontal damage than the control groups, in patients with somatoparaphrenia lesions involved, to a significantly greater extent, right orbitofrontal structures. Fig. 1 gives an overview of the extent of the observed lesions in this study superimposed on a standard outline template. We concluded that temporoparietal involvement, and presumably the resulting hemispatial neglect, were critical to the development of both asomatognosia and somatoparaphrenia, and that additional damage to the right frontal lobe, especially medial and orbitofrontal zones, may play an important contributing role. In a subsequent study, Gandola et al. (2012) compared 11 patients with and 11 without somatoparaphrenia matched for the presence or absence of neglect, motor deficits and anosognosia. Similar to the Feinberg et al. (2010) study, the somatoparaphrenia group was restricted to cases who persistently denied limb ownership and/or attributed it to someone else, and had elaborate and repeated confabulatory or delusional content. Although an asomatognosia only comparison group was not included in this study, patients with and without somatoparaphrenia were compared with a group of fifteen right brain damage patients matched for neglect, hemiplegia, and anosognosia. Gandola et al., (2012) found that somatoparaphrenia patients had large frontotemporo-parietal lesions that they interpreted as involving a neural network that is implicated in the appearance of neglect, hemiplegia and anosognosia (see Fig. 2). In this study no association between insular damage and somatoparaphrenia was found, but somatoparaphrenic patients also showed additional damage in the white matter and subcortical grey matter structures (thalamus, basal ganglia and amygdala).
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Table 1 e Reported cases of somatoparaphrenia with sufficient clinical data. Authors Sex/age Berthier and Starkstein (1987) M/63 Starkstein et al. (1990) pt. 1 M/71 Starkstein et al. (1990) pt. 2 F/48 Bisiach et al. (1991) F/84
Levine et al. (1991) pt. 4 F/78 Levine et al. (1991) pt. 6 M/60 Richardson (1992) M/64 Paulig et al. (2000) F/85 Deprati et al. (2000) M/50 Bottini et al. (2002) F/77 Moro et al. (2004) pt. S.B. M/66 Feinberg et al. (2010) pt. G1-1 M/52
pt. G1-2 M/75 pt. G1-3 M/62 pt. G1-4 F/81 Pt. G1-5 F/45 Pt. G1-6 M/53
Pt. G1-7 F/79
Fotopoulou (2011) pt. H.U. F/65 Fotopoulou (2011) pt. GR F/78 Cogliano et al. (2012) pt.G.A. M/59
Cogliano et al. (2012) pt. A.C. (M/74; left arm)
Examples of delusional misidentifications, delusions, and confabulations about paralyzed (almost exclusively) left arm Features displayed Claimed he had three left arms, one his, one his niece's and one over his chest delusions, delusional misidentification, confabulation Stated left arm “disjointed and separated”; hated it and referred to it as “jerk” delusional misidentification, misoplegia Claimed left arm was not hers, belonged to a nearby person, disliked it, hit it because it did not obey her, and referred to as “zodoquio” (neologism) delusions, delusional misidentification, confabulation, misoplegia Referred to left arm as belonging to her mother, found it in her bed, warmer than her own arm; “She forget it when she was discharged from the hospital.” Later misidentified it as her son's arm delusional misidentification, confabulation Misidentified her left arm as her husband's delusional misidentification Claimed paralyzed left arm was a “make-believe leg that his 3-year-old grandson had left in the bed when visiting earlier that day delusional misidentification, confabulation Insisted his paralyzed left arm was a “baby” delusional misidentification Referred to her left arm as her “handicapped nephew” or “a clumsy cat” delusional misidentification Claimed the left hand most likely belonged to his son delusional misidentification Claimed left hand belonged to her niece delusional misidentification Insisted the doctors had given him the arm of another patient by mistake delusional misidentification, confabulation Claimed he told my brother to remind me to take his left arm home with him or he will leave it at the hospital. Recalled saying ‘Good Lord!’ I gotta get up and pack this before I leave or I’ll leave it here” Referred to it as “a piece of useless equipment delusional misidentification, confabulation Variably misidentified the left arm as “remote control” “telephone pole” “dummy hand” delusional misidentification, confabulation Misidentified the hand as belonging to “Miss Mary's my mother-in-laws hand” delusional misidentification, confabulation Variably misidentified the hand as a “stock,” “stock option probably,” “perfume bottle” delusional misidentification Claimed the left arm was “a hand that was left on the subway and they brought it here and they put it on me” delusional misidentification, confabulation Stated “It's supposed to be my arm, but I think it's my brother's arm” He described how “gangsters chopped off his arms and threw them in the river.” It was subsequently attached to him delusional misidentification, confabulation She called the left arm a “breast” and a “deodorant” She described how her husband who had died left his hands behind. “They used to fall on my chest. I said “got to get rid of them!”. Put them in the garbage....Yes … two days ago....Still in the garbage … a black hand, with a plastic cover … you'll find them … Be careful, though … the nails are very long … and very sharp!” delusional misidentification, confabulation Claimed the left arm and leg belonged to her husband delusional misidentification Claimed the left arm belonged to her granddaughter delusional misidentification Stated that the left hand was “fake” “dead” and a third hand was replaced or added to replace the actual arm. Stated “It is third hand that my son put on me. He took it at Church because the other one does not work very well.” delusional misidentification, confabulation Stated the paralyzed right arm was a fake hand. “It doesn't listen to me. Because it is still sick, it doesn't get well yet … it is still shocked … It betrays me.” He claimed that there was an animal walking in his arm from a wound on his hand delusional misidentification, confabulation
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Table 1 e (continued ) Authors Sex/age Pugnaghi et al. (2012) F/82 Invernizzi et al. (2013) pt.C.T. F/60 Invernizzi et al. (2013) pt. G.B. F/69 Invernizzi et al. (2013) pt. A.S. F/84
Examples of delusional misidentifications, delusions, and confabulations about paralyzed (almost exclusively) left arm Features displayed Misidentified the arm as her sister's arm (who actually was in a vegetative state) She joked “I should ask my sister to pay for parking of her hand” Later referred to it as her “little hand” delusional misidentification, confabulation Complained of a “foreign, strange and short hand” in her bed abandoned by someone else delusional misidentification, confabulation Variably claimed the hand belonged to her niece Nadia, to a nurse, or another patient in the hospital delusional misidentification Referred to the hand as “foreign” and asked to have it replaced with her own “real” one that someone surely “had hidden away.” delusional misidentification, confabulation
Finally, in a recently published case series (Romano, Gandola, Bottini, & Maravita, 2014) lesion location in patients with somatoparaphrenia (but not necessarily extended and fixed delusions and confabulations) was compared with that of patients with anosognosia. In somatoparaphrenia core damage was centered in the white matter, including the corona radiata and the posterior limb of the internal capsule (Fig. 3). Damage was also detected in subcortical nuclei such as the putamen, pallidum and caudate and in the thalamus and also involved the hippocampus and amygdala, all in the right hemisphere (Romano et al., 2014). There are also a number of single case studies that are informative and provide some insight into the neuroanatomy of somatoparaphrenia. A large lesion involving frontal,
parietal and temporal cortex and both anterior and posterior insula was reported in a patient who had a severe stroke in the right hemisphere (Bartier and Starkstein, 1987). Extensive involvement of right frontal, temporal, parietal, insular cortex and subcortical white matter was found in one of the patients reported by Starkstein, Berthier, Fedoro, Price, and Robinson (1990), while another patient in the same study had a lesion more limited in extent, involving right frontal cortex and subcortical white matter. Damage in a wide area of the frontal, parietal and temporal cortex in the right hemisphere was observed in a patient who had somatoparaphrenic delusions and anosognosia (Bisiach, Rusconi, & Vallar, 1991). Right frontal or right frontal and parietal damage was reported in several cases (e.g. Bottini, Bisiach, Sterzi, & Vallar, 2002;
Fig. 1 e Areas of lesion overlap in patients with somatoparaphrenia (asomatognosia with delusions and confabulations). Lesions involved frontal, temporal, parietal and occipital cortex in the right hemisphere with more prominent damage in frontal and temporal structures than in patients with asomatognosia without somatoparaphrenic features. More specifically, in patients with somatoparaphrenia, damage extended to involve medial frontal regions. (reproduced with permission from Feinberg et al., 2010).
Fig. 2 e Areas of lesion overlap in patients with somatoparaphrenia. In patients with somatoparaphrenia there was additional and substantial damage to subcortical areas of the right hemisphere white matter extending to the posterior limb of the internal capsule, the corona radiata and the superior lateral fasciculus. Damage involved also subcortical grey matter nuclei (thalamus and basal ganglia). (reproduced with permission from Gandola et al., 2012).
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Fig. 3 e Lesions reconstruction in patients with somatoparaphrenia (but not necessarily extended and fixed delusions and confabulations). Lesion was centered in white matter in the right hemisphere and included the posterior limb of the internal capsule and the corona radiate. Damage was also identified in the basal ganglia, including caudate, putamen and pallidum, and in the thalamus. Some damage in the hippocampus and amygdala was also detected. (reproduced with permission from Romano et al., 2014).
Cogliano, Crisci, Conson, Grossi, & Trojano, 2012; Feinberg et al., 2010; Fotopoulu et al., 2011; Invernizzi et al., 2013; Jenkinson, Haggard, Ferreira, & Fotopoulou, 2013; Levine, Calvanio, & Rinn, 1991; Moro, Zampini, & Aglioti, 2004; Richardson et al., 1992). A combination of small lesions in the right motor and premotor cortex was observed in a single patient who experienced disappearance of her left arm (although this patient appeared to maintain some critical appraisal of this phenomenon) (Arzy, Overney, Landis, & Blanke, 2006) Not all cases, however, had homogeneity of damage and there are a few cases in whom the lesion extended to right temporal, occipital, subcortical white matter and thalamus (Paulig, Weber, & Garbelotto, 2000); or did not involve frontal damage (Pugnaghi, Molinar, Panzetti, Nichelli, & Zamboni, 2012) or there was additional damage in other structures such as insula (Bottini et al., 2002; Fotopoulu et al., 2011; Invernizzi et al., 2013; Jenkinson et al., 2013; Levine et al., 1991), thalamus (Daprati, Sirigu, Pradat-Diehl, Franck, & Jeannerod, 2000; Invernizzi et al., 2013; Pugnaghi et al., 2012; Paulig et al., 2000), basal ganglia (Fotopoulu et al., 2011; Invernizzi et al., 2013; Levine et al., 1991; Pugnaghi et al., 2012), and amygdala and hippocampus (Jenkinson et al., 2013). Somatoparaphrenic symptoms following left hemisphere lesions are rare, however a couple of instances are recorded in the literarure. In one case study somatoparaphrenia appeared in an ambidextrous patients following an extensive left hemisphere stroke (Ronchi et al., 2013). Somatoparaphrenia in this case occurred in the presence of language impairment typical of a left side lesion. In another case transient somatoparaphrenic symptoms appeared in a patient with a left frontoparietal meningioma (Beato, et al., 2010).
3. Theories of the etiology of somatoparaphrenia There have been a number of theories regarding the etiology of somatoparaophrenia. Somatoparaphrenia is most commonly associated with lesions of the right hemisphere
and left hemiplegia, left hemisensory defects, and visuospatial neglect. (e.g. Feinberg et al., 2010; Gandola et al., 2012; Vallar & Ronchi, 2009), Thus, hemispatial neglect certainly plays a contributory role. As hemispatial neglect commonly involves damage to temporoparietal cortex (see Verdon, Schwartz, Lovblad, Hauert, and Vuilleumier (2010) for instance) it is expected that any study of asomatognosia or somatoparaphrenia will show damage to these sectors. A variety of other neuropsychological symptoms may also be associated with somatoparaphrenic delusions. Diminished attentional capacity is often seen in patients with this type of delusion and an association with sensory and proprioceptive impairments and perturbed body representations has been reported. Others investigators have posited disruption of processes related to self-representation that leads to an alienation of the limb and the related confabulatory, bizarre and fixed delusional manifestations typical of somatoparaphrenia. (Feinberg et al., 2010). The latter approach also emphasizes the interaction of neuropsychological, motivational and psychodynamic factors (Feinberg, 2010, 2011, 2013). Other cognitive accounts include: a deficit of multisensory integration and of spatial representation of the body (Vallar & Ronchi, 2009); “DSO” linked to posterior insular damage (Baier & Karnath, 2008); and a neurogenic dissociation between the “subjectively felt” (first person) and “objectively seen” (third person) body perspectives (Fotopoulou, et al., 2011); reduction of the sense of familiarity for the paralyzed limb (Gandola et al., 2012); and an impairment in body/space interaction with reduction in reactivity to harmful stimuli and consequent reduction of monitoring of that ‘safety zone’ around one's own body (Romano et al., 2014). The latter theory posits that in these cases there is a reduced response to sensory threats approaching the body and an altered physiological index of perceptual analysis. A dissociation between intact body ownership and disrupted sensory awareness in turn suggests that body representation might be disrupted at different levels (Romano et al., 2014). When an interpretation of somatoparaphrenia has been offered outside the field of neurology and neuropsychology,
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some authors have argued that it is not possible to account for the appearance of this symptom only in terms of impairment of ownership of body parts, but that there should be an adequate account of the phenomenology of this symptom and a distinction should be made between the feeling of ownership of a body part and the feeling of ownership of a specific experience which refers to that body part (Liang & Lane, 2009). It is suggested that somatoparaphrenia might appear through a process of misidentification due to immunity to error in a very restricted area of the self (Rosenthal, 2005). In this framework the self is a combination of personal history, physical and psychological features and current circumstances, features which all together contribute to selfidentification, a process which in some instances can fail (Rosenthal, 2004). However, this account has been criticized on the basis that it does not fully account for cases who misattribute conscious sensations to a third party (e.g. Bottini et al., 2002). Some authors have reconciled this apparent inconsistency by suggesting a possible dissociation between the presence of a conscious sensation and a higher order representation of that sensation (Lane & Liang, 2010). One issue when considering whether the productive aspects of somatoparaphrenia are related to damage to a specific neuroanatomical structure is that, in most instances, somatoparaphrenia appears in patients who have overall larger lesions when compared with patients with only neglect, anosognosia, or those who lack extensive delusions and confabulations (Feinberg et al., 2010) or neglect without somatoparaphrenia (Gandola et al., 2012). In addition, current lesion analysis approaches may not be sufficiently accurate to identify, if not in broad terms, the precise anatomical structures that, when damaged, disconnected or dysfunctional might facilitate the emergence of delusional phenomena related to the paralyzed limb. Furthermore, more studies of somatoparaphrenia are needed in which parameters of disruption of functional and structural connectivity within the cortex are quantitatively measured. It is possible that more advanced imaging techniques via their ability to detect subtle dysfunction either in cortical activity or white matter functioning might be more sensitive and precise in identifying disruption in crucial brain areas, or networks, that might generate delusional manifestations involving the paralysed limb. In the latter case it is possible that specific disruption might occur between structures associated with sensory processing and body representations which are part of the default mode network (Raichle, et al., 2001) and those that are part of a “salience network” (Seeley et al., 2007) whose structures are primarily involved in the early cognitive control of behaviorally salient events such as internally generated signal errors (Ham, et al., 2013). Insular cortex and anterior cingulate cortex are integral parts of the salience network and there is evidence that interactions of the dorsal anterior cingulate cortex play a key role in moment to moment adjustments in behavioral control; furthermore, changes in effective connectivity between the insula and the dorsal anterior cingulate cortex appear to disrupt activity in more posterior brain structures (Ham, Leff, de Boissezon, Joffe, and Sharp, 2013). In addition, the evidence from cases in which partial resolution of symptoms was obtained through
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vestibular stimulation (e.g., Ronchi et al., 2013) or some other stimulation technique suggests that somatoparaphrenic symptoms are not necessarily the outcome of a structural lesion, but might be the result of a functional deficit which might be transient or which can be temporarily restored by stimulation in appropriate regions associated with body representation. Finally, as in many other instances of confabulation, somatoparaphrenia may not be explained solely on the basis of lesion location alone. The possible contribution of motivational variables toward the tendency to confabulate and delusional thoughts towards the affected limb cannot be disregarded. There are other instances of spontaneous confabulations which have been explained in terms of a patient's attempt to overcome unpleasant events and reality with the creation of false beliefs which are more pleasant than real events (Feinberg, DeLuca, Giacino, Roane, & Solms, 2005; Feinberg & Roane, 1997; Fotopoulou, Solms, & Turnbull, 2004; Shanks, McGeown, Guerrini, & Venneri, 2014). A holistic approach involving neuroanatomical, cognitive and neuropsychoanalytical explanations in combination has to be invoked to reach a better understanding of this symptom's development following brain damage (Feinberg, 2010, 2011, 2013).
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Feinberg, T. E. (2009). From axons to identity: Neurological explorations of the nature of the self. New York: W.W. Norton. Feinberg, T. E. (2010). Neuropathologies of the self: a general theory. Neuropsychoanalysis, 12, 133e158. Feinberg, T. E. (2011). Neuropathologies of the self: clinical and anatomical features. Consciousness and Cognition, 20, 75e81. Feinberg, T. E. (2013). Neuropathologies of the self and the right hemisphere: a window into productive personal pathologies. Frontiers in Human Neuroscience, 7, 472. Feinberg, T. E., DeLuca, J., Giacino, J. T., Roane, D. M., & Solms, M. (2005). Right hemisphere pathology and the self: delusional misidentification and reduplication. In T. E. Feinberg, & J. P. Keenan (Eds.), The Lost Self: Pathologies of the Brain and Identity (pp. 100e130). Oxford, UK: Oxford University Press. Feinberg, T. E., & Roane, D. M. (1997). Anosognosia, completion and confabulation: the neutral e personal dichotomy. Neurocase, 3, 73e85. Feinberg, T. E., Venneri, A., Simone, A. M., Fan, Y., & Northoff, G. (2010). The neuroanatomy of asomatognosia and somatoparaphrenia. Journal of Neurology, Neurosurgery, and Psychiatry, 81, 276e281. Fotopoulou, A., Jenkinson, P. M., Tsakiris, M., Haggard, P., Rudd, A., & Kopelman, M. D. (2011). Mirror-view reverses somatoparaphrenia: dissociation between first- and thirdperson perspectives on body ownership. Neuropsychologia, 49, 3946e3955. Fotopoulou, A., Solms, M., & Turnbull, O. (2004). Wishful reality distortions in confabulation: a case report. Neuropsychologia, 42, 727e744. , E. R., Sterzi, R., Gandola, M., Invernizzi, P., Sedda, A., Ferre Sberna, M., et al. (2012). An anatomical account of somatoparaphrenia. Cortex, 48, 1165e1178. Gerstmann, J. (1942). Problem of imperception of disease and of impaired body territories with organic lesions. Archives of Neurology and Psychiatry, 48, 890e913. Halligan, P. W., Marshall, J. C., & Wade, D. T. (1995). Unilateral somatoparaphrenia after right hemisphere stroke: a case description. Cortex, 31, 173e182. Ham, T. E., de Boissezon, X., Leff, A., Beckmann, C., Hughes, E., Kinnunen, K. M., et al. (2013a). Distinct frontal networks are involved in adapting to internally and externally signaled errors. Cerebral Cortex, 13, 703e713. Ham, T., Leff, A., de Boissezon, X., Joffe, A., & Sharp, D. J. (2013b). Cognitive control and the salience network: an investigation of error processing and effective connectivity. The Journal of Neuroscience, 33, 7091e7098. Invernizzi, P., Gandola, M., Romano, D., Zapparoli, L., Bottini, G., & Paulesu, E. (2013). What is mine? Behavioral and anatomical dissociations between somatoparaphrenia and anosognosia for hemiplegia. Behavioral Neurology, 26, 139e150. Jenkinson, P. M., Haggard, P., Ferreira, N. C., & Fotopoulou, A. (2013). Body ownership and attention in the mirror: insights from somatoparaphrenia and the rubber hand illusion. Neuropsychologia, 51(8), 1453e1462. Lane, T., & Liang, C. (2010). Mental ownership and higher-order thought: response to rosenthal. Analysis, 70, 496e501.
Levine, D. N., Calvanio, R., & Rinn, W. E. (1991). The pathogenesis of anosognosia for hemiplegia. Neurology, 41, 1770e1781. Liang, C., & Lane, T. (2009). Higher-order thought and pathological self: the caseof somatoparaphrenia. Analysis, 69, 661e668. Loetscher, T., Regard, M., & Brugger, P. (2006). Misoplegia. A review of the literature and a case without hemiplegia. Journal of Neurology, Neurosurgery and Psychiatry, 77, 1099e1100. Moro, V., Zampini, M., & Aglioti, S. M. (2004). Changes in spatial position of hands modify tactile extinction but not disownership of contralesional hand in two right braindamaged patients. Neurocase, 10, 437e443. Paulig, M., Weber, M., & Garbelotto, S. (2000). Somatoparaphrenie. Eine “plusvariante” der Anosognosie fu¨r Hemiplegie. Nervenartz, 71, 123e129. Pearce, J. M. (2007). Misoplegia. European Neurology, 57, 62e64. Pugnaghi, M., Molinar, M., Panzetti, P., Nichelli, P. F., & Zamboni, G. (2012). “My sister's hand is in my bed”: a case of somatoparaphrenia. Neurological Science, 33, 1205e1207. Raichle, M. E., MacLeod, A. M., Snyder, A. Z., Powers, W. J., Gusnard, D. A., & Shulman, G. L. (2001). A default mode of brain function. Proceedings of the National Academy of Sciences of the United States of America, 98, 676e682. Richardson, J. K. (1992). Psychotic behavior after right hemispheric cerebrovascular accident: a case report. Archives of Physical Medicine and Rehabilitation, 73, 381e384. , A., Rossetti, Y., & JacquinRonchi, R., Rode, G., Cotton, F., Farne Courtois, S. (2013). Remission of anosognosia for right hemiplegia and neglect after caloric vestibular stimulation. Restorative Neurology and Neuroscience, 31, 19e24. Romano, D., Gandola, M., Bottini, G., & Maravita, A. (2014). Arousal responses to noxious stimuli in somatoparaphrenia and anosognosia: clues to body awareness. Brain, 137, 1213e1223. Rosenthal, D. M. (2004). Being conscious of ourselves. The Monist, 87, 161e184. Rosenthal, D. M. (2005). Consciousness and mind. New York: Oxford University Press. Seeley, W. W., Menon, V., Schatzberg, A. F., Keller, J., Glover, G. H., Kenna, H., et al. (2007). Dissociable intrinsic connectivity networks for salience processing and executive control. Journal of Neuroscience, 27, 2349e2356. Shanks, M. F., McGeown, W. J., Guerrini, C., & Venneri, A. (2014). Awareness and confabulation. Neuropsychology, 28, 406e414. http://dx.doi.org/10.1037/neu0000031. Starkstein, S. E., Berthier, M. L., Fedoro, V. P., Price, T. R., & Robinson, R. G. (1990). Anosognosia and major depression in 2 patients with cerebrovascular lesions. Neurology, 40, 1380e1382. Vallar, G., & Ronchi, R. (2009). Somatoparaphrenia: a body delusion. A review of the neuropsychological literature. Experimental Brain Research, 192, 533e551. Verdon, V., Schwartz, S., Lovblad, K. O., Hauert, C. A., & Vuilleumier, P. (2010). Neuroanatomy of hemispatial neglect and its functional components: a study using voxel-based lesion-symptom mapping. Brain, 133, 880e894.
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Special issue: Review
Somatoparaphrenia: Evolving theories and concepts Todd E. Feinberg a,* and Annalena Venneri b a Departments of Psychiatry and Neurology, Icahn School of Medicine at Mount Sinai and the Yarmon Neurobehavior and Alzheimer's Disease Center, Mount Sinai Beth Israel, New York, NY, USA b Department of Neuroscience, University of Sheffield, UK and IRCCS San Camillo Foundation Hospital, Venice, Italy
article info
abstract
Article history:
Somatoparaphrenia, a syndrome that involves at a minimum unawareness of ownership
Received 1 December 2013
of a body part, in addition involves productive features including delusional misidentifi-
Reviewed 22 January 2014
cation and confabulation. In this review we describe some of the clinical and neuroana-
Revised 26 February 2014
tomical features of somatoparaphrenia highlighting its delusional and confabulatory
Accepted 1 July 2014
aspects. Possible theoretical frameworks are reviewed taking into account cognitive, psy-
Published online 22 July 2014
chodynamic, and philosophical views. We suggest that future studies should approach this syndrome through investigations of structural and functional connectivity and focus on
Keywords:
the possible interplay between alterations in major functional networks of the brain, such
Somatoparaphrenia
as the default mode and salience networks, but also take into account motivational
Asomatognosia
variables.
Delusional misidentification
© 2014 Elsevier Ltd. All rights reserved.
Confabulation Self-boundaries
1.
Asomatognosia and somatoparaphrenia
After Babinski first coined the term “anosognosia” (1914, 1918), Gerstmann (1942) suggested that there were three “indirect disorders of the body scheme” that were characterized by an abnormal experience of, behavior toward, or verbal statements about a function of or part of the body. In all three of these conditions, the most common clinical presentation involves an abnormal attitude toward the left arm in the setting of right hemisphere damage, or deficit of awareness for left hemiplegia, hemisensory deficits and hemispatial neglect
(Critchley, 1953; 1955; Feinberg, Haber, & Leeds, 1990; Feinberg, Venneri, Simone, Fan, & Northoff, 2010; Feinberg, 2009; Gerstmann, 1942; Halligan, Marshall, & Wade, 1995; Vallar & Ronchi, 2009). The first of these was anosognosia itself (lack of knowledge of disease) referred to by Gerstmann as “cases of imperception of disease or defect in function” (1942, p. 909). Second were cases of “imperception of the defective parts or side of the body, with forgetting of their existence or non recognition of their possession” (1942, p. 909). It was this condition that Critchley (1953) later called asomatognosia (“lack of knowledge of the body”). The third syndrome Gerstmann (1942) called
* Corresponding author. Yarmon Neurobehavior and Alzheimer's Disease Center, Mount Sinai Beth Israel, 1st Avenue at 16th Street, New York, NY 10003, USA. E-mail address: [email protected] (T.E. Feinberg). http://dx.doi.org/10.1016/j.cortex.2014.07.004 0010-9452/© 2014 Elsevier Ltd. All rights reserved.
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somatoparaphrenia, which was essentially a variant of asomatognosia involving delusional beliefs about the contralesional side of the body: “For the condition predominating in cases of the third group, I believe the designation somatoparaphrenia to be suitable, since it takes account of the fact that in the negative state of experience of absence of a certain part or area of the body, induced by disease, positive psychopathological phenomena in the sphere of the body scheme are apt to occur” (Gerstmann, 1942, p. 909). According to Gerstmann (1942), in somatoparaphrenia, the experience of absence of the affected limb is associated with “illusional, confabulatory or delusional ideas of a peculiar nature” (p. 909). Critchley (1955) later added, among the more common features of somatoparaphrenia, personification of the paralyzed limbs in which the contralesional limbs are conferred a separate identity and may be said to belong to a relative, a child or a pet (Critchley, 1953, 1955; 1974; Feinberg, 2009; Feinberg et al., 2010), and misoplegia (Critchley, 1974; Loetscher, Regard, & Brugger, 2006; Pearce, 2007) in which the limb is hated, abused, or physically attacked (Table 1; See Vallar and Ronchi (2009) for a comprehensive review of some additional descriptive distinctions). This review will focus mainly on those cases and group studies in which somatoparaphrenic delusions were the most prominent symptoms, and were accompanied by confabulations. A description of a sample of these cases is shown in Table 1.
2.
The neuroanatomy of somatoparaphrenia
In the first large study of the neuroanatomy of asomatognosia, Feinberg et al. (1990) compared 12 patients with right hemisphere strokes, asomatognosia, and hemispatial neglect with 4 patients with neglect but without asomatognosia. For the purposes of this study, any patient who verbally denied ownership of the limb was deemed to display asomatognosia whether or not delusions or confabulations were present. Thus, these cases included both Gerstmann's second type (Critchley's asomatognosia), and Gerstmann's third type (somatoparaphrenia). This study reported damage to the supramarginal gyrus in the inferior parietal lobule and its subcortical connections within the posterior corona radiata to be the most common lesions in these cases and were significantly more common than in a control group of patients with right hemisphere lesions and hemispatial neglect but without asomatognosia of any form. In the next group study, Baier and Karnath (2008) studied “disturbed sensation of limb ownership” (DSO) in a group of 12 right hemisphere damaged patients with anosognosia for hemiplegia. DSO designated a fairly broad group of symptoms and included cases of somatoparaphrenia, misoplegia, and personification of the limb, but also cases of anosodiaphoria, kinesthetic hallucinations, and supernumerary phantom limb, the latter symptoms not traditionally designated within the somatoparaphrenia syndrome. In this broad group they found that 11/12 (91.7%) patients demonstrated DSO, and within this group damage to right posterior insula was the
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critical region. However, in that study cases of somatoparaphrenia were not independently analyzed from cases of anosodiaphoria, kinesthetic hallucinations, and supernumerary phantom limb. The Feinberg et al. (1990) study did not distinguish between patients with asomatognosia and those with somatoparaphrenia, the latter specifically including cases with confabulation, delusions, delusional misidentifications, or personifications of the limb. These two syndromes have significant clinical distinctions and to see whether these differences were associated with significant neuroanatomical differences, Feinberg et al. (2010) compared cases with simple asomatognosia (asomatognosia only group) who showed unelaborated errors regarding the ownership of the limb, to cases with somatoparaphrenia who had asomatognosia plus extensive delusions, misidentifications, and confabulations regarding the limb and controls with hemispatial neglect but neither asomatognosia or somatoparaphrenia. In this study we found that all patients with asomatognosia only or somatoparaphrenia, as well as controls, had significant temporoparietal involvement or, less commonly, damage to other structures such as the insula that have been implicated in the feeling of ownership of the limb (Baier & Karnath, 2008). Thus, involvement of posterior temporoparietal regions was critical to the establishment of both asomatognosia and somatoparaphrenia. However, patients with somatoparaphrenia had the overall largest lesions and significantly more right medial frontal involvement than patients with simple asomatognosia. Furthermore, while patients with asomatognosia only had more medial frontal damage than the control groups, in patients with somatoparaphrenia lesions involved, to a significantly greater extent, right orbitofrontal structures. Fig. 1 gives an overview of the extent of the observed lesions in this study superimposed on a standard outline template. We concluded that temporoparietal involvement, and presumably the resulting hemispatial neglect, were critical to the development of both asomatognosia and somatoparaphrenia, and that additional damage to the right frontal lobe, especially medial and orbitofrontal zones, may play an important contributing role. In a subsequent study, Gandola et al. (2012) compared 11 patients with and 11 without somatoparaphrenia matched for the presence or absence of neglect, motor deficits and anosognosia. Similar to the Feinberg et al. (2010) study, the somatoparaphrenia group was restricted to cases who persistently denied limb ownership and/or attributed it to someone else, and had elaborate and repeated confabulatory or delusional content. Although an asomatognosia only comparison group was not included in this study, patients with and without somatoparaphrenia were compared with a group of fifteen right brain damage patients matched for neglect, hemiplegia, and anosognosia. Gandola et al., (2012) found that somatoparaphrenia patients had large frontotemporo-parietal lesions that they interpreted as involving a neural network that is implicated in the appearance of neglect, hemiplegia and anosognosia (see Fig. 2). In this study no association between insular damage and somatoparaphrenia was found, but somatoparaphrenic patients also showed additional damage in the white matter and subcortical grey matter structures (thalamus, basal ganglia and amygdala).
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Table 1 e Reported cases of somatoparaphrenia with sufficient clinical data. Authors Sex/age Berthier and Starkstein (1987) M/63 Starkstein et al. (1990) pt. 1 M/71 Starkstein et al. (1990) pt. 2 F/48 Bisiach et al. (1991) F/84
Levine et al. (1991) pt. 4 F/78 Levine et al. (1991) pt. 6 M/60 Richardson (1992) M/64 Paulig et al. (2000) F/85 Deprati et al. (2000) M/50 Bottini et al. (2002) F/77 Moro et al. (2004) pt. S.B. M/66 Feinberg et al. (2010) pt. G1-1 M/52
pt. G1-2 M/75 pt. G1-3 M/62 pt. G1-4 F/81 Pt. G1-5 F/45 Pt. G1-6 M/53
Pt. G1-7 F/79
Fotopoulou (2011) pt. H.U. F/65 Fotopoulou (2011) pt. GR F/78 Cogliano et al. (2012) pt.G.A. M/59
Cogliano et al. (2012) pt. A.C. (M/74; left arm)
Examples of delusional misidentifications, delusions, and confabulations about paralyzed (almost exclusively) left arm Features displayed Claimed he had three left arms, one his, one his niece's and one over his chest delusions, delusional misidentification, confabulation Stated left arm “disjointed and separated”; hated it and referred to it as “jerk” delusional misidentification, misoplegia Claimed left arm was not hers, belonged to a nearby person, disliked it, hit it because it did not obey her, and referred to as “zodoquio” (neologism) delusions, delusional misidentification, confabulation, misoplegia Referred to left arm as belonging to her mother, found it in her bed, warmer than her own arm; “She forget it when she was discharged from the hospital.” Later misidentified it as her son's arm delusional misidentification, confabulation Misidentified her left arm as her husband's delusional misidentification Claimed paralyzed left arm was a “make-believe leg that his 3-year-old grandson had left in the bed when visiting earlier that day delusional misidentification, confabulation Insisted his paralyzed left arm was a “baby” delusional misidentification Referred to her left arm as her “handicapped nephew” or “a clumsy cat” delusional misidentification Claimed the left hand most likely belonged to his son delusional misidentification Claimed left hand belonged to her niece delusional misidentification Insisted the doctors had given him the arm of another patient by mistake delusional misidentification, confabulation Claimed he told my brother to remind me to take his left arm home with him or he will leave it at the hospital. Recalled saying ‘Good Lord!’ I gotta get up and pack this before I leave or I’ll leave it here” Referred to it as “a piece of useless equipment delusional misidentification, confabulation Variably misidentified the left arm as “remote control” “telephone pole” “dummy hand” delusional misidentification, confabulation Misidentified the hand as belonging to “Miss Mary's my mother-in-laws hand” delusional misidentification, confabulation Variably misidentified the hand as a “stock,” “stock option probably,” “perfume bottle” delusional misidentification Claimed the left arm was “a hand that was left on the subway and they brought it here and they put it on me” delusional misidentification, confabulation Stated “It's supposed to be my arm, but I think it's my brother's arm” He described how “gangsters chopped off his arms and threw them in the river.” It was subsequently attached to him delusional misidentification, confabulation She called the left arm a “breast” and a “deodorant” She described how her husband who had died left his hands behind. “They used to fall on my chest. I said “got to get rid of them!”. Put them in the garbage....Yes … two days ago....Still in the garbage … a black hand, with a plastic cover … you'll find them … Be careful, though … the nails are very long … and very sharp!” delusional misidentification, confabulation Claimed the left arm and leg belonged to her husband delusional misidentification Claimed the left arm belonged to her granddaughter delusional misidentification Stated that the left hand was “fake” “dead” and a third hand was replaced or added to replace the actual arm. Stated “It is third hand that my son put on me. He took it at Church because the other one does not work very well.” delusional misidentification, confabulation Stated the paralyzed right arm was a fake hand. “It doesn't listen to me. Because it is still sick, it doesn't get well yet … it is still shocked … It betrays me.” He claimed that there was an animal walking in his arm from a wound on his hand delusional misidentification, confabulation
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Table 1 e (continued ) Authors Sex/age Pugnaghi et al. (2012) F/82 Invernizzi et al. (2013) pt.C.T. F/60 Invernizzi et al. (2013) pt. G.B. F/69 Invernizzi et al. (2013) pt. A.S. F/84
Examples of delusional misidentifications, delusions, and confabulations about paralyzed (almost exclusively) left arm Features displayed Misidentified the arm as her sister's arm (who actually was in a vegetative state) She joked “I should ask my sister to pay for parking of her hand” Later referred to it as her “little hand” delusional misidentification, confabulation Complained of a “foreign, strange and short hand” in her bed abandoned by someone else delusional misidentification, confabulation Variably claimed the hand belonged to her niece Nadia, to a nurse, or another patient in the hospital delusional misidentification Referred to the hand as “foreign” and asked to have it replaced with her own “real” one that someone surely “had hidden away.” delusional misidentification, confabulation
Finally, in a recently published case series (Romano, Gandola, Bottini, & Maravita, 2014) lesion location in patients with somatoparaphrenia (but not necessarily extended and fixed delusions and confabulations) was compared with that of patients with anosognosia. In somatoparaphrenia core damage was centered in the white matter, including the corona radiata and the posterior limb of the internal capsule (Fig. 3). Damage was also detected in subcortical nuclei such as the putamen, pallidum and caudate and in the thalamus and also involved the hippocampus and amygdala, all in the right hemisphere (Romano et al., 2014). There are also a number of single case studies that are informative and provide some insight into the neuroanatomy of somatoparaphrenia. A large lesion involving frontal,
parietal and temporal cortex and both anterior and posterior insula was reported in a patient who had a severe stroke in the right hemisphere (Bartier and Starkstein, 1987). Extensive involvement of right frontal, temporal, parietal, insular cortex and subcortical white matter was found in one of the patients reported by Starkstein, Berthier, Fedoro, Price, and Robinson (1990), while another patient in the same study had a lesion more limited in extent, involving right frontal cortex and subcortical white matter. Damage in a wide area of the frontal, parietal and temporal cortex in the right hemisphere was observed in a patient who had somatoparaphrenic delusions and anosognosia (Bisiach, Rusconi, & Vallar, 1991). Right frontal or right frontal and parietal damage was reported in several cases (e.g. Bottini, Bisiach, Sterzi, & Vallar, 2002;
Fig. 1 e Areas of lesion overlap in patients with somatoparaphrenia (asomatognosia with delusions and confabulations). Lesions involved frontal, temporal, parietal and occipital cortex in the right hemisphere with more prominent damage in frontal and temporal structures than in patients with asomatognosia without somatoparaphrenic features. More specifically, in patients with somatoparaphrenia, damage extended to involve medial frontal regions. (reproduced with permission from Feinberg et al., 2010).
Fig. 2 e Areas of lesion overlap in patients with somatoparaphrenia. In patients with somatoparaphrenia there was additional and substantial damage to subcortical areas of the right hemisphere white matter extending to the posterior limb of the internal capsule, the corona radiata and the superior lateral fasciculus. Damage involved also subcortical grey matter nuclei (thalamus and basal ganglia). (reproduced with permission from Gandola et al., 2012).
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Fig. 3 e Lesions reconstruction in patients with somatoparaphrenia (but not necessarily extended and fixed delusions and confabulations). Lesion was centered in white matter in the right hemisphere and included the posterior limb of the internal capsule and the corona radiate. Damage was also identified in the basal ganglia, including caudate, putamen and pallidum, and in the thalamus. Some damage in the hippocampus and amygdala was also detected. (reproduced with permission from Romano et al., 2014).
Cogliano, Crisci, Conson, Grossi, & Trojano, 2012; Feinberg et al., 2010; Fotopoulu et al., 2011; Invernizzi et al., 2013; Jenkinson, Haggard, Ferreira, & Fotopoulou, 2013; Levine, Calvanio, & Rinn, 1991; Moro, Zampini, & Aglioti, 2004; Richardson et al., 1992). A combination of small lesions in the right motor and premotor cortex was observed in a single patient who experienced disappearance of her left arm (although this patient appeared to maintain some critical appraisal of this phenomenon) (Arzy, Overney, Landis, & Blanke, 2006) Not all cases, however, had homogeneity of damage and there are a few cases in whom the lesion extended to right temporal, occipital, subcortical white matter and thalamus (Paulig, Weber, & Garbelotto, 2000); or did not involve frontal damage (Pugnaghi, Molinar, Panzetti, Nichelli, & Zamboni, 2012) or there was additional damage in other structures such as insula (Bottini et al., 2002; Fotopoulu et al., 2011; Invernizzi et al., 2013; Jenkinson et al., 2013; Levine et al., 1991), thalamus (Daprati, Sirigu, Pradat-Diehl, Franck, & Jeannerod, 2000; Invernizzi et al., 2013; Pugnaghi et al., 2012; Paulig et al., 2000), basal ganglia (Fotopoulu et al., 2011; Invernizzi et al., 2013; Levine et al., 1991; Pugnaghi et al., 2012), and amygdala and hippocampus (Jenkinson et al., 2013). Somatoparaphrenic symptoms following left hemisphere lesions are rare, however a couple of instances are recorded in the literarure. In one case study somatoparaphrenia appeared in an ambidextrous patients following an extensive left hemisphere stroke (Ronchi et al., 2013). Somatoparaphrenia in this case occurred in the presence of language impairment typical of a left side lesion. In another case transient somatoparaphrenic symptoms appeared in a patient with a left frontoparietal meningioma (Beato, et al., 2010).
3. Theories of the etiology of somatoparaphrenia There have been a number of theories regarding the etiology of somatoparaophrenia. Somatoparaphrenia is most commonly associated with lesions of the right hemisphere
and left hemiplegia, left hemisensory defects, and visuospatial neglect. (e.g. Feinberg et al., 2010; Gandola et al., 2012; Vallar & Ronchi, 2009), Thus, hemispatial neglect certainly plays a contributory role. As hemispatial neglect commonly involves damage to temporoparietal cortex (see Verdon, Schwartz, Lovblad, Hauert, and Vuilleumier (2010) for instance) it is expected that any study of asomatognosia or somatoparaphrenia will show damage to these sectors. A variety of other neuropsychological symptoms may also be associated with somatoparaphrenic delusions. Diminished attentional capacity is often seen in patients with this type of delusion and an association with sensory and proprioceptive impairments and perturbed body representations has been reported. Others investigators have posited disruption of processes related to self-representation that leads to an alienation of the limb and the related confabulatory, bizarre and fixed delusional manifestations typical of somatoparaphrenia. (Feinberg et al., 2010). The latter approach also emphasizes the interaction of neuropsychological, motivational and psychodynamic factors (Feinberg, 2010, 2011, 2013). Other cognitive accounts include: a deficit of multisensory integration and of spatial representation of the body (Vallar & Ronchi, 2009); “DSO” linked to posterior insular damage (Baier & Karnath, 2008); and a neurogenic dissociation between the “subjectively felt” (first person) and “objectively seen” (third person) body perspectives (Fotopoulou, et al., 2011); reduction of the sense of familiarity for the paralyzed limb (Gandola et al., 2012); and an impairment in body/space interaction with reduction in reactivity to harmful stimuli and consequent reduction of monitoring of that ‘safety zone’ around one's own body (Romano et al., 2014). The latter theory posits that in these cases there is a reduced response to sensory threats approaching the body and an altered physiological index of perceptual analysis. A dissociation between intact body ownership and disrupted sensory awareness in turn suggests that body representation might be disrupted at different levels (Romano et al., 2014). When an interpretation of somatoparaphrenia has been offered outside the field of neurology and neuropsychology,
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some authors have argued that it is not possible to account for the appearance of this symptom only in terms of impairment of ownership of body parts, but that there should be an adequate account of the phenomenology of this symptom and a distinction should be made between the feeling of ownership of a body part and the feeling of ownership of a specific experience which refers to that body part (Liang & Lane, 2009). It is suggested that somatoparaphrenia might appear through a process of misidentification due to immunity to error in a very restricted area of the self (Rosenthal, 2005). In this framework the self is a combination of personal history, physical and psychological features and current circumstances, features which all together contribute to selfidentification, a process which in some instances can fail (Rosenthal, 2004). However, this account has been criticized on the basis that it does not fully account for cases who misattribute conscious sensations to a third party (e.g. Bottini et al., 2002). Some authors have reconciled this apparent inconsistency by suggesting a possible dissociation between the presence of a conscious sensation and a higher order representation of that sensation (Lane & Liang, 2010). One issue when considering whether the productive aspects of somatoparaphrenia are related to damage to a specific neuroanatomical structure is that, in most instances, somatoparaphrenia appears in patients who have overall larger lesions when compared with patients with only neglect, anosognosia, or those who lack extensive delusions and confabulations (Feinberg et al., 2010) or neglect without somatoparaphrenia (Gandola et al., 2012). In addition, current lesion analysis approaches may not be sufficiently accurate to identify, if not in broad terms, the precise anatomical structures that, when damaged, disconnected or dysfunctional might facilitate the emergence of delusional phenomena related to the paralyzed limb. Furthermore, more studies of somatoparaphrenia are needed in which parameters of disruption of functional and structural connectivity within the cortex are quantitatively measured. It is possible that more advanced imaging techniques via their ability to detect subtle dysfunction either in cortical activity or white matter functioning might be more sensitive and precise in identifying disruption in crucial brain areas, or networks, that might generate delusional manifestations involving the paralysed limb. In the latter case it is possible that specific disruption might occur between structures associated with sensory processing and body representations which are part of the default mode network (Raichle, et al., 2001) and those that are part of a “salience network” (Seeley et al., 2007) whose structures are primarily involved in the early cognitive control of behaviorally salient events such as internally generated signal errors (Ham, et al., 2013). Insular cortex and anterior cingulate cortex are integral parts of the salience network and there is evidence that interactions of the dorsal anterior cingulate cortex play a key role in moment to moment adjustments in behavioral control; furthermore, changes in effective connectivity between the insula and the dorsal anterior cingulate cortex appear to disrupt activity in more posterior brain structures (Ham, Leff, de Boissezon, Joffe, and Sharp, 2013). In addition, the evidence from cases in which partial resolution of symptoms was obtained through
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vestibular stimulation (e.g., Ronchi et al., 2013) or some other stimulation technique suggests that somatoparaphrenic symptoms are not necessarily the outcome of a structural lesion, but might be the result of a functional deficit which might be transient or which can be temporarily restored by stimulation in appropriate regions associated with body representation. Finally, as in many other instances of confabulation, somatoparaphrenia may not be explained solely on the basis of lesion location alone. The possible contribution of motivational variables toward the tendency to confabulate and delusional thoughts towards the affected limb cannot be disregarded. There are other instances of spontaneous confabulations which have been explained in terms of a patient's attempt to overcome unpleasant events and reality with the creation of false beliefs which are more pleasant than real events (Feinberg, DeLuca, Giacino, Roane, & Solms, 2005; Feinberg & Roane, 1997; Fotopoulou, Solms, & Turnbull, 2004; Shanks, McGeown, Guerrini, & Venneri, 2014). A holistic approach involving neuroanatomical, cognitive and neuropsychoanalytical explanations in combination has to be invoked to reach a better understanding of this symptom's development following brain damage (Feinberg, 2010, 2011, 2013).
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