Alien Hand Syndrome
KeywordsVoluntary Movement Primary Motor Cortex Progressive Supranuclear Palsy Efference Copy Alien Limb
Short Description or Definition
Alien hand syndrome (AHS) is a relatively rare manifestation of damage to specific brain regions involved in purposive voluntary movement. It is postulated to be an impairment of the “sense of agency” or, alternatively, an impairment of intentionality. The core observation is the patient report that one of his/her hands is displaying purposeful, coordinated, and goal-directed behavior over which the patient feels he/she has no direct voluntary control. The patient fails to recognize the action of one of their hands as their own. The hand, effectively, appears to manifest a “will of its own.” This unique involuntary movement disorder is characterized by coordinated, well-organized, and clearly goal-directed limb movements that would otherwise be indistinguishable from normal voluntary movement. This definition excludes disordered, non-purposeful, and dyskinetic movements associated with other involuntary movement disorders such as chorea, athetosis, hemiballism, and myoclonus.
The alien hand can be engaged in performing a specific goal-directed task or the purposeful use of an external object. Distinguishing this condition from asomatognosia, there is typically normal awareness and recognition of the limb reported by the patient. However, the patient perceives a lack of self-agency (“I am not doing that…”) with regard to the observed behavior of the limb but displays an intact “sense of ownership” (“…even though I know this is my hand”). While the original description of this condition occurred in patients with well-defined focal lesions of cerebral cortex, with the majority of cases due to cerebral infarction, it has since been described in a variety of different clinical conditions including corticobasal syndrome, progressive supranuclear palsy, Alzheimer’s disease, and Creutzfeldt-Jakob disease. Furthermore, while the alien limb is typically and most often noted in an upper extremity, it has been described in the lower extremity as well.
This suggests that the alien hand syndrome reflects a phenomenon that may result from impaired function at a variety of different points in a widely distributed brain system involved in the intentional preparation and generation of purposeful voluntary movement. This system would be expected to include both specifically defined motor and premotor regions of the cerebral cortex as well as related interconnected subcortical regions such as the basal ganglia. The different clinical variants of AHS associated with circumscribed cortical damage which will be reviewed below may reflect varying clusters of clinical manifestations resulting from disrupted functions at different points and levels within this distributed brain system. As noted, this distributed brain system would be expected to involve a variety of both cortical and associated subcortical regions engaged together in the emerging brain process linked to voluntary movement generation, with the common pathophysiologic manifestation being a dissociation between self-perceived will and action.
One of the significant difficulties in conceptualizing and studying AHS in the context of a conventional scientific paradigm is that a mechanistic explanation alone cannot adequately account for the process linked to intentionality and the teleological aspect of goal-directed behavior. The emerging field of “biosemiotics” that recognizes the process of semiosis through which meaning and action-associated intentionality emerge in the behavior of living organisms promises to provide a new perspective and, in the process, provide potential insights into this disorder.
Two major forms of AHS can be distinguished. One form is related to focal cortical and intercortical white matter damage and the other is associated with more diffusely distributed cortical/subcortical damage (e.g., as seen in corticobasal syndrome). Three variants of the focal cortical form of AHS have been described, each with unique behavioral manifestations and neuroanatomical correlations. These variants include the frontal, callosal, and posterior forms.
The most common variant is the “frontal” form. It is typically associated with damage to the medial surface of the cerebral hemisphere in the frontal region. This variant has been described in cerebral infarction in the territory of the anterior cerebral artery, with tumors involving the medial surface of the cerebral hemisphere, and in other conditions affecting the function of the medial frontal lobe region. When the region of injury extends posteriorly to involve the medial aspect of the prefrontal gyrus associated with the primary motor cortex (PMC), the patient may present with crural hemiparesis, with greater weakness in the leg as compared to the arm. This presentation corresponds to the topographical organization of the PMC with control of lower limb movement located more medially than the areas on the exterior lateral surface that control the upper limb and face. The frontal variant is seen with involvement of the medial aspect of the premotor cortex anterior to PMC including the pre-supplementary (pre-SMA) and supplementary motor area (SMA), and anterior cingulate cortex (ACC), as well as connections to the posterior cingulate cortex (PCC). In functional activation studies, the medial frontal cortex has also been found to activate spontaneously with complex purposeful movements and with internal imaging of voluntary movement, suggesting that it may serve as a higher-level system that modulates the activation of PMC in accordance with volitional features of the performance. The readiness potential, or Bereitschaftspotential, a slowly developing surface-negative shift that precedes an overt voluntary movement by over 1200 ms, arises through activation of the anteromedial frontal cortex, suggesting that excitation of this system precedes the appearance of the overt movement and activation of the PMC. Activation of the ACC is involved in intentional suppression of prepotent responses as tested with the Stroop test. These areas may serve as a higher-level system modulating the activation of PMC in accordance with the volitional self-referenced aspects of the performance. Alternatively, they may be part of a feed-forward system that generates an efference copy of the generated motor command that is transmitted to sensory cortex as a means of distinguishing active self-generated limb movement with its associated sensory re-afference, from passive movement produced by external forces associated with sensory ex-afference.
Behaviors seen frequently with the frontal variant include involuntary, visually driven reaching and grasping onto objects, an inability to voluntarily release these objects, and utilization behavior in which the presence of a frequently encountered object used in daily activities such as a comb or a toothbrush elicits behavior in which the object may be put to use independent of the general interpersonal context. A grasp reflex to tactile stimulation is often present in the affected hand. The patient may wake themselves up from sleep by grasping onto and pulling at their own body parts. Patients may show a prepotent tendency to be drawn toward external objects. They also may demonstrate alien-associated sexual self-stimulation or involuntary fondling of another’s body, a great source of public embarrassment (Ong Hai and Odderson 2000). Interestingly, while the patient clearly manifests purposeful involuntary coordinated behaviors in the affected limb that appear to flow effortlessly, attempts to willfully move the limb are effortful and arduous. Voluntary movement in the affected limb is often hypokinetic and hypometric with greater activation of the axial and proximal limb muscles compared to the distal muscles controlling the wrist and fingers, even though these muscles are fully and dexterously activated in the alien movements. Generally, these alien behaviors appear in the hand contralateral to the damaged hemisphere regardless of hemispheric dominance. When the dominant hemisphere is damaged, in addition to alien hand behavior in the dominant hand, they may experience difficulty with the initiation of spontaneous speech while still being able to follow verbal commands and repeat phrases without difficulty. These findings are consistent with a transcortical motor aphasia that affects spontaneous verbalization and production of propositional speech more than repetition and generally responsive language output. Alternatively, this has been interpreted as a partial mutism manifesting as an inability to initiate spontaneous propositional verbal output.
The “callosal” variant is seen with an isolated lesion of the corpus callosum. The voluntary motor systems of the two hemispheres are isolated from each other due to lost interhemispheric communication resulting in impaired intermanual coordination. This variant has been described most frequently as a transient condition following callosotomy in the treatment of intractable seizures. It may also be seen following infarction or tumors selectively involving the corpus callosum.
In the “callosal” variant of AHS, the appearance of “intermanual conflict” or “self-oppositional” behaviors is the predominant feature. Grasping behaviors and externally driven reaching movements seen in the frontal variant are notably less prominent. When there is a major disconnection between the two hemispheres resulting from callosal injury, the language-linked dominant hemispheric agent that maintains its primary control over the contralateral dominant limb effectively loses its direct and linked control over the separate “agent” based in the nondominant hemisphere (and, thus, the nondominant limb), which had been previously responsive and “obedient” to the dominant agent. The possibility of purposeful action in the nondominant limb occurring outside of the realm of influence of the dominant agent thus can occur. In the callosal variant, the problematic alien hand is consistently the nondominant hand, while the dominant hand is the identified “good” normally controlled hand. The patient may express frustration and bewilderment at the conflicting and disruptive behavior of the alien hand whose motivations remain inaccessible to consciousness. There may be an attentional component that modulates the appearance of these episodes of self-oppositional behavior since intermanual conflict is observed more frequently when the patient is fatigued, stressed, or is engaged in effortful multitasking and divided-attention activity. Occasionally, rather than acting in a contradictory manner, the two hands are observed to be engaged in two different and entirely unrelated activities as if being guided by completely separate and independent intentions.
In a dramatic example of this behavior, one patient was observed to initiate smoking a cigarette by pulling the cigarette out of the package and placing it in her mouth with the controlled dominant hand followed by the alien nondominant hand, rather than beginning to light the cigarette, suddenly reaching up, pulling it out of her mouth, and throwing it across the room. Astonished, the patient reasoned that perhaps the alien hand was not in favor of her smoking!
The callosal and frontal variants are often seen in combination with a corresponding overlap of observed behaviors. For example, following cerebral infarction in the territory of the anterior cerebral artery, there may be ischemic injury to both the medial frontal lobe and the corpus callosum. In this circumstance, there may be both visually directed reaching and grasping alien behaviors in the limb contralateral to the area of injury as well as episodes of intermanual conflict. However, a clear differentiation between apparent intermanual conflict due to attempts to restrain alien behaviors associated with the frontal variant (e.g., as in the case of “self-grasping” described below), and true intermanual conflict, in which the two hands are directed toward independently contradictory purposes, may be difficult to differentiate.
Posterior or “Sensory” Variant
The third identified variant of AHS is the “posterior” or “sensory” form, which appears most often with a parietal or parieto-occipital focus of circumscribed damage. As in the frontal variant, the alien behavior appears in the hand contralateral to the damaged hemisphere.
In the patient with the posterior variant, the movement of the affected alien limb is typically less organized and often has an ataxic instability particularly with visually guided reaching. The limb also may show proprioceptive sensory impairment with hypesthesia, so that kinesthetic impairment limits the monitoring of limb position. Visual field deficits as well as hemi-inattention may be seen on the same side as the alien hand. In this variant, the limb may be observed to lift up off of support surfaces involuntarily and “levitate” in the air seemingly to avoid contact between the palmar surface of the affected hand and support surfaces. It may also be seen to withdraw from objects approaching the hand in distinct contrast to the reaching and grasping behaviors that are seen in the frontal variant. The alien hand may assume a characteristic posture of fully extended digits with the palmar surface retreating from environmental objects, and support surfaces an observation that has been labeled an “instinctive avoidance reaction” by Denny-Brown and has also been referred to as a “parietal hand.” At times, grasping behaviors can also be observed with the posterior variant.
Alien hand behavior has also been reported in association with focal subcortical thalamic infarction.
Distributed Cortical/Subcortical Form
In addition to having been observed in the context of stroke, tumors, and callosotomy, alien hand behavior has been described in a second general form linked to degenerative neurological conditions that tend to affect cortical and subcortical regions together. The progressive neurodegenerative disorders associated with this form of AHS include corticobasal syndrome, progressive supranuclear palsy, multiple sclerosis, spongiform encephalopathy, and Alzheimer’s disease. When AHS appears with these progressive encephalopathies, it is usually accompanied by various forms of motor apraxia, along with multiple additional cognitive and motor disturbances characteristic of the particular condition.
While there are no epidemiologic studies of the occurrence of AHS variants in association with acquired brain damage, it can be assumed that this is a relatively rare but striking manifestation of neurologic pathology.
Pathophysiology and Prognosis
Adapting the concept developed by Derek Denny-Brown regarding positive and negative cortical tropisms based in the parietal lobe and frontal lobes (Denny-Brown 1956, 1966), respectively, a heuristic model has been proposed. In this model, there are two separable but interactive components of an intrahemispheric premotor intentional system that modulate the output of the PMC of the hemisphere and its direct influence via the corticospinal tract over the spinal motor nuclei innervating the distal muscles of the contralateral limbs (Goldberg and Bloom 1990).
The common factor in these anomalous conditions is the relative sparing of the PMC region controlling the contralesional alien hand, while the premotor regions involved in the intentional selection of action and the inhibition of automatic behaviors in response to external factors are impaired. A recent fMRI study of cortical activation patterns associated with alien and non-alien movement has demonstrated that alien movement is in fact characterized by isolated activation of PMC without concomitant activation of intrahemispheric premotor regions, while voluntary behavior includes the activation of PMC in concert with activation of intrahemispheric premotor regions (Assal et al. 2007).
Neuropsychology and Psychology of AHS
The presence of AHS can cause the patient significant psychological distress as the hand seems to possess the capability for acting autonomously, independent of their conscious voluntary control. The patient may become fearful that they will be held accountable for consequences of an action of the alien hand over which they do not feel control. The patient may display “autocriticism” complaining that the alien hand is not doing what it has been “told to do” and is therefore characterized as disobedient, wayward, or “evil.” The hand is felt to be under the control of an external unknown agent to whose narrative and intentions the patient is not privy. They may even physically strike the alien hand with the controlled hand as a “punishment” intended to discourage its wayward behavior, or restrain the movement of the alien hand by grasping tightly onto it with the controlled hand (“self-grasping”). They may verbally address and instruct the hand as if it were an unruly child acting autonomously and in need of disciplinary intervention. Conversely, they may respond to these contrary actions with amusement.
Given the predicament created, the patient may develop depersonalization and dissociate themselves from the unintended actions of the hand. They often choose to identify an external “alien” source for the voluntary control of the hand, or assign a distinct personality to the hand as a way of seeking a satisfactory narrative to explain this perplexing and disturbing situation.
From a psychological perspective, it is helpful to counsel the patient regarding the organic basis of their problem and provide assurance that there is a rational explanation for their concerns and that there is evidence that these problems can be treated and are likely to gradually improve over time.
In AHS, different regions of the brain are able to command purposeful limb movements, without generating the conscious feeling of self-control over these movements. There is thus a dissociation between the actual execution of the physical movements of the limb and the process that produces an internal sense of voluntary control over the movements. This latter process, impaired in AHS, normally produces the conscious sense of agency that conveys that the movement is being internally initiated and produced by an active self. Presumably, this process differentiates reliably between “re-afference” (i.e., the return of kinesthetic sensation from the self-generated “active” limb movement) and “ex-afference” (i.e., kinesthetic sensation generated from an externally produced “passive” limb movement). It may do this by giving rise to a parallel output signal from motor regions, a so-called efference copy. The efference copy is then translated into a corollary discharge, which conveys the expected re-afferent sensory response from the commanded movement. The corollary discharge can then be used in somatosensory cortex as a referent to distinguish re-afference from ex-afference and thus differentiate a self-produced active movement from a passive movement resulting from external forces. AHS may thus involve impaired production and transmission of either an efference copy or a corollary discharge signal.
Evaluation of the patient with AHS involves careful observation of limb movement in various naturalistic contexts, along with reports from the patient regarding their sense of control over these movements. The relative dependence of movement on external context should be evaluated through assessment for utilization behaviors elicited by the presentation of external objects commonly encountered in daily activities. A phenomenological approach to assessing and documenting the motor behavior and linking it to introspective first-person report of the patient’s own experience is essential. Not only should the verbal reports of the patient be noted but also the associated affect. The limb should be evaluated for evidence of a grasp reflex with both tactile and visual stimulation. The ability to release objects that have been grasped should also be assessed. Evaluation for callosal apraxia and impairment of interhemispheric transfer of information should be included. When the posterior variant of AHS is suspected, a visual field assessment and careful sensory examination of the affected limb should be completed as well as assessment for hemi-inattention. Evidence of an avoidant tendency to withdraw the limb from tactile and visual stimulation should also be elicited and noted when present.
There is no definitive specific treatment for AHS but a number of different rehabilitative approaches have been described. Furthermore, in the presence of unilateral damage within a single cerebral hemisphere, there is often a gradual reduction in the frequency of alien behaviors observed over time and a gradual restoration of normal voluntary control over the affected hand. This suggests that neuroplasticity in the bihemispheric and subcortical brain systems involved in voluntary movement production can serve to reestablish functional connection between the executive production process and the internal self-generation and volitional registration process. Exactly how this may occur is not well understood but could involve a reorganization within residual elements of the intrahemispheric premotor systems both at the cortical and subcortical levels. In addition, some degree of expanded participation of the intact ipsilateral hemisphere may be involved in the recovery process by extending ipsilateral motor projections and influence.
Different strategies can be used to reduce the interference of the alien hand behavior in the ongoing coherent controlled functional actions of everyday life being performed by the patient. In the frontal variant, an object such as a cane can be placed in the grip of the alien hand so that it does not reach out to grasp onto other objects, thus impeding the patient’s forward progress during walking. In another approach, voluntary control of the limb is developed by training the patient to perform a specific task with the alien limb, such as moving the alien hand to contact a specific object or a highly salient environmental target. Through training to enhance volitional control, the patient can effectively override the alien behavior when it occurs. Recognizing that alien behaviors in the frontal variant are often sustained by tactile input, another approach involves simultaneously “muffling” the actions of the alien hand and limiting sensory feedback by placing it in a restrictive “cloak” such as a specialized soft foam hand orthosis or, alternatively, an everyday oven mitt. Of course, this then limits the degree to which the hand can engage in functional tasks. It may also be possible to develop improved participation of ipsilateral hemispheric premotor mechanisms by engaging the patient in coordinated bimanual activities that necessitate cooperative coherent coordinative mechanisms within residual intact components of the motor control systems in both hemispheres.
References and Readings
- Bakheit, A. M., Brennan, A., Gan, P., Green, H., & Roberts, S. (n.d.). Anarchic hand syndrome following resection of a frontal lobe tumor. Neurocase, 19, 36–40.Google Scholar
- Brugger, F., Galovic, M., Weder, B. J., & Kägi, G. (2015). Supplementary motor complex and disturbed motor control. A retrospective clinical and lesion analysis of patients after anterior cerebral artery syndrome. Frontiers in Neurology. doi: 10.3389/fneur.2015.00209. Available online at: http://journal.frontiersin.org/article/10.3389/fneur.2015.00209/full.
- Denny-Brown, D. (1966). The cerebral control of movement. Liverpool: Liverpool University Press.Google Scholar
- Hoffmeyer, J. (2011). The natural history of intentionality. A biosemiotic approach. In T. Schilhab, F. Stjernfelt, & T. Deacon (Eds.), Biosemiotics vol. 6: The symbolic species evolved (pp. 97–116). New York: Springer.Google Scholar
- Sarva, H., Deik, A., & Severt, W. L. (2014). Pathophysiology and treatment of alien hand syndrome. Tremor and Other Hyperkinetic Movements, 4, 241. 10.7916/D8VX0F48. Available online at: http://www.tremorjournal.org/index.php/tremor/article/view/241
- Synofzik, M., Vosgerau, G., & Newen, A. (n.d.). I move, therefore I am: A new theoretical framework to investigate agency and ownership. Consciousness and Cognition, 17, 411–424.Google Scholar
- Wolfe, N., Moore, J. W., Rae, C. L., Rittman, T., Altena, E., Haggard, P., & Rowe, J. B. (2013). The medial frontal-prefrontal network for altered awareness and control of action in corticobasal syndrome. Brain, 137, 208–220.Google Scholar