The dynamic nature of the sense of ownership after brain injury. Clues from asomatognosia and somatoparaphrenia

Highlights

• We revised all the cases of somatoparaphrenia (SP) described in the literature.

• We presented three new peculiar cases of SP.

• None of primary sensory-motor deficit is likely necessary for SP.

• We proposed a new theoretical framework to explain SP.

• We discussed SP as a deficit of the dynamic update of body-space information.

Abstract

The sense of ownership is the feeling that a body part belongs to ourselves. Brain damage may disrupt this feeling, leading to somatoparaphrenia (SP), i.e., the delusion that one's limbs belong to someone else. This delusional feeling is typically associated with profound motor and somatosensory deficits.

We reviewed the cases of SP reported so far in the literature outlining the clinical and neuroanatomical profile of SP. We then investigated and reported three new peculiar cases of SP that allow new insights into the theoretical framework of this neuropsychological condition. We thus propose an innovative theoretical account that integrates previous evidence and the new cases described. We suggest that a defective update of the ongoing dynamic representation of the body finalised to perception and action, may be the key for the disownership feelings of patients with SP. The erroneous spatial representation of the limb contralateral to the lesion would have the logical consequence of delusional misattribution of the seen own arm.

Introduction

Our body, the object we know the best (de Vignemont, 2011), holds very complex and dedicated representations in the brain, being a unique reference for sensory-motor experiences (Berlucchi & Aglioti 1997, 2010).

The feeling that a given body part belongs to ourselves is a fundamental aspect of the neural representation of the body: this is typically defined as the sense of ownership and is an implicit, essential, determinant of any current sensory or motor event (Romano et al., 2015b). Brain damage may dramatically disrupt body ownership, leading to a number of symptoms, among which the most striking is somatoparaphrenia (de Vignemont, 2011). Somatoparaphrenia (SP) is a neuropsychological condition characterised by delusional feelings about the patient's own body (Gerstmann, 1942; Giuseppe Vallar and Ronchi, 2009; Feinberg and Venneri, 2014).

SP is rather uncommon, typically observed in the acute post-ictal phase and characterised by the illusory sense of disownership of the patient's contralesional limbs. Crucially, in SP, the denied limbs are attributed to other individuals that are typically around the patient during the examination – e.g., caregivers and relatives (Gandola et al., 2012; Invernizzi et al., 2013; Feinberg et al., 2010). Sometimes the ownership misattribution involves someone who is not, or could not possibly be currently present (Pugnaghi et al., 2011; Bottini et al., 2002). The presence of a ownership misattribution is a key element distinguishing SP from asomatognosia, a different impairment of sense of ownership that is carachterised by the failure of having a continuous sensation, feeling or judgment that one's body part (typically the impaired limb) belongs to the patient (Jenkinson et al., 2018). In other words, SP features dense sense of disownership toward the impaired limb (asomatognosia), coupled with delusional attribution of that limb to someone else.

The neurological and cognitive processes impaired in SP are still to be further clarified. As far as the associated neurological symptoms, it is clear that isolated hemiplegia or hemianesthesia cannot fully account for the presence of SP, given that most patients affected by profound sensory and motor deficits are not somatoparaphrenic. However, the impact of each of these neurological symptoms on SP needs further investigation. As far as the cognitive mechanisms, on one side SP has been attributed to a disruption of the conscious and stable features of the body representation. Those features are responsible for the explicit attribution of limb ownership, the so-called body image, likely favoured by severe motor and proprioceptive deficits (Daprati et al., 2010; Geschwind, 1965). On the other side, it was recently proposed that spatial and dynamic aspects of body representation, the so-called body schema, may have a crucial impact in the occurrence of SP (Romano et al., 2014; Salvato et al., 2016; Vallar and Ronchi, 2009).

In the present paper, we first provide a comprehensive and critical review of published cases of SP (N = 130). A key aspect is the focus on the association of SP with other neurological deficits and on the dynamic relation of delusional feelings of the patients to the space around them. This particular view of SP suggests considering such a striking phenomenon in a dynamic body-space relation. This theoretical framework seems to be supported by the investigation of three particular cases of SP, which are reported for the first time in this paper. We thus propose a novel theoretical framework for understanding SP in light of previous theories and the new cases.

Specific case descriptions of SP can be tracked back at the end of XIX Century (see Anton 1893 reported in Vallar and Ronchi, 2009), but systematic investigations of altered body representation and their putative neurological underpinnings have been reported in the seminal work by Head and Holmes in 1911, where the concept of body schema was formally introduced. With Gerstmann (1942) and his first definition of SP, the new fundamental question about the neurological nature of the sense of body ownership was raised, becoming a central issue of neuropsychology and cognitive neuroscience (Critchley, 1953; Vallar and Coslett, 2018).

Although SP is a rare condition, its potential contribution to the understanding of the physiological and pathological sense of ownership is undoubted. In the present section of the paper, we provide an operative definition of SP that allows identifying a large homogeneous group of patients among all those described in the literature.

In the seminal work by Gerstmann, (1942) two patients were reported who presented with a sense of disownership for one arm which they attributed to someone else. This deficit was not isolated since the same patients concurrently showed a pathological embodiment of other people's limbs in their own body (Gerstmann, 1942). The initial definition of SP incorporated a varied group of symptoms, including the denial of ownership of an affected body part, but also several other conditions which were considered part of the same core deficit. These conditions included misoplegia (i.e. the aversive behaviour toward the affected limb), anosognosia (i.e. the unawareness of neurological deficits), and other milder signs of extraneity for body parts (Critchley, 1953). However, all those additional deficits do not necessarily hold the same underlying cognitive mechanisms and neural substrates, calling for the necessity of a sharper definition of SP (Jenkinson et al., 2018).

SP can be currently defined as an acquired condition characterised by the delusional belief that a body part does not belong to one's own body (i.e., asomatognosia (Jenkinson et al., 2018)), and is attributed to someone else. Those beliefs do not depend on a generalised delirium or psychiatric disorder (Fotopoulou et al., 2011; Gandola et al., 2012; Romano et al., 2014; Feinberg and Venneri, 2014; de Vignemont, 2011; Jenkinson et al., 2018), but to a modular disruption of consciousness, selectively targeted to a single body part or body side (Bisiach et al., 1991; Bottini et al., 2002). We used this operative definition of SP to identify the cases of SP in the literature.