Somatoparaphrenia (SP) lacks ownership of a paralyzed limb, i.e., the illusion that one leg belongs to another [1]. SP is one of the many forms of body misperception, an uncommon, pervasive neuropsychological disorder consisting of delusional sensation in the absence of a confusional state. Body misperceptions include asomatognosia (lack of awareness of a body part), the experience of supernumerary phantom limbs, personification (naming a limb and giving it an identity of its own) and misoplegia. This latter term was coined by Critchley and coll, and it refers to the morbid dislike or hatred of paralyzed limbs [1]. Body misperceptions can result from a brain injury in the parietal, frontal or insular cortex [2], which interrupts and damages a correct body representation (BR), also leading to profound motor and somatosensory deficits [3]. BR is defined as the mental representation of one’s body. It results from the integration of multisensory information (visual, sensory, vestibular, and proprioceptive) with the pre-existing knowledge of the individual [4, 5, 6, 7]. Thus, BR consists of perception, memory, and cognition related to the body and is continuously updated by sensory inputs due to brain plasticity, reorganizing a different body perception due to internal and external feedback [5, 6, 8, 9, 10, 11]. In recent years, some authors have highlighted that SP arises from lesions of specific cortical areas mainly located in the right hemisphere and involving the radiated crown and some subcortical gray matter structures [12, 13, 14]. In particular, the frontotemporal-parietal regions are connected to the integrity of one’s body and the BR [7, 15].

Recent studies have hypothesized that the repudiation of the patients’ body parts with SP is due to deficits in the ongoing dynamic representation of the body involved in perception and action. Thus, the incorrect spatial representation of the contralateral limb to the lesion would result from an erroneous delusional attribution of one’s limb [3]. SP presupposes a failure of the brain multisensory areas with an odd sense of possessing a body: this is the reason why Blanke [16] suggests a deficit in coherent multisensory integration that allows for adequate bodily self-awareness. More in detail, SP (like other alterations of body self-awareness) could be due to integration disturbances between proprioceptive, interoceptive, and vestibular signals on body position and movement with visual signals from the body.

SP and the primary body representation disorders have no specific and standardized rehabilitation approach [2]. SP and misoplegia tend to regress spontaneously within a few days or weeks. In some cases, however, the disorder tends to persist, negatively affecting the rehabilitation of motor and sensory functions. Hence, an increase in awareness of the limbs is necessary to facilitate the patient’s recovery. Due to the clinical complexity of these cases, Feinberg & Venneri [17] underlined that an approach including cognitive, neuroanatomical, psychological, and motor components could help promote a patient’s recovery. Indeed, there is insufficient evidence of positive outcomes for such patients in the literature. Rehabilitation consists mainly of behavioral methods that allow the patient to explore his/her body (use of suggestions, mirror, and verbal commands) [18, 19, 20, 21]. Indeed, some authors have observed that the modulation of sensory signals by caloric vestibular stimulation [18, 19, 20] and visual inspection of the renegade limb in a mirror [21] could reduce the delusions due to SP.

SP and the other form of body misperceptions, such as misoplegia are complex conditions, which affects the patient’s clinical recovery and his/her quality of life. Then, such disorders should be rehabilitated using a holistic approach, as both socio-psychological and biological factors contribute to their complex etiopathogenesis. The aim of the study was the development of a new protocol to rehabilitate body misperception. We managed a patient who complained of right hemiparesis with SP and misoplegia after a neurosurgical intervention, using a novel multidisciplinary approach.

A 50-year-old, right-handed, Italian woman attended our Institute (in day hospital regimen) from June to September 2019, owing to a right hemiparesis after a neurosurgical intervention for a left parietal meningioma (occurred in March 2019). She was an English/French teacher and an unmarried translator and lived with her 80-year-old mother. Her family and personal history were negative for neurological and psychiatric disorders.

At the admission, the patient presented with difficulty standing in the upright position, abnormal gait and right moderate hemiparesis, mainly involving the lower limb. No alteration of proprioception or sense of vibration was observed. No cognitive deficits were reported after the surgical intervention and during the rehabilitation period in another Hospital. However, when reviewing her past rehab history, we found that the patient systematically refused the exercises focused on her lower limb. No one investigated the reason why she behaved this way. The patient also reported that this was the first time she talked about this problem. A brain MRI scan revealed the results of the parietal vertex craniotomy, with the surgical cavity surrounded by peripheral gliotic reaction and Wallerian degeneration of the left corticospinal tract. No Gadolinium enhancement was appreciable (Fig. 1).

Fig. 1.

Brain MRI scan showing the results of the parietal vertex craniotomy, with the surgical cavity (red line delimited area) surrounded by peripheral gliotic reaction (green line delimited area) and Wallerian degeneration of the left corticospinal tract (yellow arrow).

At the end of the multidisciplinary approach, the neuropsychological evaluation showed improved cognitive functioning and reduced anxiety (Table 2). In addition, the human figure test and BUT showed that the patient changed her BR and the perception of herself and her body, without any sense of estrangement and repulsion for the right lower limb (Table 3). In particular, we observed a drastic change in the human figure drawn in the HFT (Fig. 2). Initially, the figure was stylized, with few details, other than the extremities of the limbs (hands and feet) represented by circles. We also notice a difference in representing the two feet, and the right one appears larger and more angular than the left foot in both figures (male and female). At the end of the training, the figure was represented with different details, including clothing, feet with shoes, and well-defined hands. The pencil trait was safer, the drawings occupied the entire page, and the differences between the two feet were reduced (Fig. 2). The patient also noticed these aspects at the end of the HFT. From a motor point of view, the articular excursion of the right tibiotarsal joint improved and the patient’s stability and endurance during walking. However, it was performed with the aid of a cane. Moreover, at the end of the training, we observed improving all cognitive domains (Table 2).

Fig. 2.

Female (A) and male (B) Human Figure Test the baseline (left picture) and at the end of the training (right picture).

At baseline, the first analysis showed increased neural responsiveness in a large cluster covering the right frontoparietal areas, including premotor, motor, and somatosensory cortex. Following the rehabilitation training, we found a more focused activation over the sensory areas, particularly those of the lower limbs (Fig. 3).

Concerning the second analysis, we did not find any significant differences in brain activation following the stimulation of each limb at either baseline or post-intervention.

Last, there was right hemisphere lateralization of cortical activations within the motor areas at baseline, modified in a bilateral motor activation post-intervention (Fig. 3).

Fig. 3.

Representation of the brain areas with statistically significant activations (Z scores on the color bar) on 19-channel analysis in the omega range (full band: 1–45 Hz). eLORETA was used to analyze the cortical distribution of the current source density during bilateral lower limb sensory stimulation (SS) and bilateral stepping motor task (MT) at pre- and post-intervention.

The patient we described complained of a rare condition, i.e., SP as a surgical outcome of benign tumor lesions. SP following brain lesions usually tends to recover spontaneously in a few days or a few weeks, whereas the symptoms persisted for months and were underrated in our patient. Furthermore, the patient had a left-hemisphere lesion, adding another piece of rarity. Most patients with SP have indeed a lesion in the right hemisphere [32]. Notwithstanding, the assessment and management of bodily misperception, including SP and misoplegia, remains challenging regardless of the pathological basis of the bodily misperception [32]. Therefore, to find new approaches to improve bodily perception should be welcomed [33].

Our case report raises awareness on two main issues concerning bodily misperception. First, the assessment of bodily misperception requires an appropriate neuropsychological investigation in patients with parietal lesions, even when anosognosia and neglect are not clinically evident. Indeed, SP was misdiagnosed before the patient came to our attention, and the diagnosis was fundamental to the patient’s tailored treatment. Second, we have used an advanced approach to better manage bodily misperception management.

As previously stated, there are currently no standardized treatments for body-awareness disorders, especially for SP and misoplegia. Considering that these disorders often regress spontaneously, there is not much attention in the rehab setting. Nonetheless, some studies suggest using awareness-raising therapies, such as providing information on paretic body parts or touching the body parts involved in the neuropsychological deficit [2, 34]. Behavioral or physiological methods, such as vestibular caloric stimulation, have led to controversial results. Recently, Dieguez and Lopez have observed that to better understand this pathology, it could be helpful to use virtual reality, robotics, and neuroprosthetics to learn more about the neural mechanisms involved [35]. On this basis, we decided to combine various rehabilitative approaches: the conventional methods, such as psychological support, physiotherapy, and body exploration and innovative methods, such as robotics, to further potentiate the patient’s recovery. Innovative technology has proven effective in patients with BR disorders [36, 37].

Our innovative protocol effectively improved body perception and motor outcomes, thus highlighting the importance of a multidisciplinary approach to treat SP efficiently. For the first time, this case report shows that the combination of intensive motor training (both conventional and robotic) and PC could be a practical approach for SP rehabilitation. PC allowed the patient to acquire more awareness of her body as a whole, thanks to “auto-observation” work, enabling her to modify the dysfunctional thoughts about herself and the syndrome. Indeed, the changes reported in the HFT and the BUT scales might indicate a reconstruction of the process of body awareness, with the re-appropriation of oneself and a sense of bodily belonging. These changes are likely due to the opportunity to verbalize the patient’s feelings and the knowledge about her negative emotional experiences, allowing to consider the foot as an integrated part of the body. In addition, traditional physiotherapy coupled with robotic training influenced the patient’s outcomes. Indeed, the intensive, task-oriented, and repetitive motor practice probably boosted some neural plasticity mechanisms consistently with the principles of sensorimotor integration [38, 39]. Notably, Kalron et al. [40] proposed that cognitive and motor processes are based on shared circuits; therefore, an integrated rehabilitation approach may affect cognitive, sensory and motor processes, favoring the right functionality of the involved circuits.

The concomitant EEG findings also suggest this. Indeed, the patient showed an apparent deficit of activation within the sensorimotor areas within the affected hemisphere and an activation overflow within the unaffected hemisphere. This phenomenon may be consistent with a deteriorated interhemispheric inhibition; actually, a parietal lesion can negatively affect such mechanisms by deteriorating the frontoparietal connectivity related to parietal-lobe-driven cognitive processes [41, 42]. Furthermore, the parietal damage and the consequent frontoparietal network impairment may account for an overflowing integration activity within the frontoparietal cortical networks to the detriment of the segregation processes [43, 44]. This last aspect is suggested by the lack of any significant difference in brain activation following the stimulation of each limb. Overall, the imbalance between segregation and integration within different frontoparietal networks resulting from a parietal lesion could have distorted BR. We can only hypothesize this pathophysiological scenario, given that many other structures, including the posterior visuomotor area and limbic system, come into play concerning BR [45, 46].

Notwithstanding, our results confirm that the delusions in SP may depend on an altered physiological index of perceptual analysis [10]. Our data point out an apparent impairment in the somatosensory processing of sensory stimuli directed to the contralesional limb compared to those directed to the ipsilesional limb. This is consistent with what has been observed in SP patients by using anticipatory skin conductance response. It seems different from what has been found in control individuals and patients with anosognosia for the somatosensory deficit and with pure motor deficits. These data further support that BR may be affected at different levels following brain damage [10].

Beyond these pathophysiological aspects, the interhemispheric imbalance we found was partially recovered by the combined approach; the magnitude of this change makes the hypothesis that the patient’s improvement occurred by chance unlikely. Interhemispheric imbalance recovery also favored a reduction of the right hemisphere lateralization of the cortical activations within the motor areas to a more functional bilateral activation while stepping bilaterally. This issue is of noticeable importance in gait rehabilitation, as it is a fundamental requirement for gait recovery [47]. To summarize, the multisensory stimulation carried out by multidisciplinary and integrated training could have improved BR changes, with an increase in both the motor and cognitive domains. This finding could indicate that BR is an issue that should be considered in rehabilitation programs. It can be modified through environmental stimulation and could also affect the patient’s motor and psychological outcomes. Furthermore, our approach positively impacted both SP and misoplegia contemporary. This is not of negligible importance, as these disorders are distinct entities, although belonging to the same spectrum, and they have different neurophysiological bases [18, 48]. SP has been considered a variant or severe form of anosognosia for hemiplegia for many years [49].

Our patient did not show anosognosia for hemiplegia. In line with Sakamoto et al. [48], we found that anosognosia for hemiplegia, personal neglect, and somatosensory disorder is not required to diagnose SP.Moreover, the patient presented with SP from a left-sided lesion, which is rare [32]. These unique SP features may explain why the syndrome was not diagnosed before the patient came to our observation. Indeed, there is a predominance of the right hemisphere regarding body representation and somatic attention [50]. However, lesions of the left hemisphere may also cause neglect and related disorders, often associated with aphasia or comprehension abnormalities [51]. Some authors showed that SP could be explained by multisensory integration areas, essential for body ownership and BR sensation. Thus, the dysfunction of these regions, regardless of the hemisphere involved, could produce symptoms of limb dis-ownership [52, 53]. The neural correlates of SP involve specific brain areas, including the parietal and temporal lobe and dorsolateral frontal cortex, which are essential for the BR [3, 7, 9, 12, 13, 54, 55, 56].

Consequently, a brain injury in these areas affects the BR and the planning and motor execution skills based on these body representations [7, 57, 58]. This may result in deficits in movement planning, performance, control and imagination, mental rotation, body part position, body part naming, and tools related to body parts [57, 59]. Rehabilitation strategies aimed at targeting BR deterioration can be helpful to improve BR itself and motor outcomes [60].

We acknowledge that our findings are limited by the lack of a comparison of previous treatment strategies and a control group. However, the clinical picture we described is uncommon and challenging to compare. Moreover, given that the spontaneous recovery occurs mainly within the first months after the symptom onset, it is unlikely that this may have happened in our patient, who was treated in the late subacute stage. Therefore, any preliminary approach to managing SP and misoplegia contemporary should be welcomed as in our patient. Notwithstanding, our results suggest that an integrated psychological and motor approach may effectively rehabilitate patients with SP, even in the presence of misoplegia. Further studies with larger samples should be conducted to confirm our promising results.

A, Avoidance; B I, Mouth; B II, Face Shape; B III, Thighs; B IV, Legs; B V, Harms; B VI, Moustache; B VII, Skin; B VIII, Blushing; BDI II, Beck Depression Inventory-II; BIC, Body Image Concern; BR, Body Representation; BUT-A, Body Uneasiness Test (part A); BUT-B, Body Uneasiness Test (part B); CSM, Compulsive Self-Monitoring; D, Depersonalization; FAB, Frontal Assessment Battery; FIM, Functional Independence Measure; GSI, Global Severity Index; HRS-A, Hamilton Rating Scale for Anxiety; LL, Ashworth scale Lower Limb; MoCA, Montreal Cognitive Assessment; PC, Psychological Counseling; PSDI, Positive Symptom Distress Index; PST, Positive Symptom Total; RCI, Reliable Change Index; SP, Somatoparaphrenia; WP, Weight Phobia.

These should be presented as follows: MGM, AN, RSC and GLR designed the research study. MGM, PC, GLR, BP, DL, PM performed the research. AN analyzed the data. MGM, PC, RSC and AN wrote the manuscript. All authors contributed to editorial changes in the manuscript. All authors read and approved the final manuscript.

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards. The Institutional Review Board of IRCCS Centro Neurolesi Bonino Pulejo (Messina, Italy) approved the study. Patients provided their written informed consent to study participation and data publication.

Not applicable.

This research received no external funding.

Given his role as the Editorial Board Member of JIN, Prof. Rocco Salvatore Calabrò had no involvement in the peer-review of this article and has no access to information regarding its peer-review.