Disappearance of “phantom limb” and amputated arm usage during dreaming in REM sleep behaviour disorder

Abstract

Limb amputation is followed, in approximately 90% of patients, by “phantom limb” sensations during wakefulness. When amputated patients dream, however, the phantom limb may be present all the time, part of the time, intermittently or not at all. Such dreaming experiences in amputees have usually been obtained only retrospectively in the morning and, moreover, dreaming is normally associated with muscular atonia so the motor counterpart of the phantom limb experience cannot be observed directly. REM sleep behaviour disorder (RBD), in which muscle atonia is absent during REM sleep and patients act out their dreams, allows a more direct analysis of the “phantom limb” phenomena and their modifications during sleep.

BACKGROUND

Limb amputation is followed, in approximately 90% of patients, by “phantom limb” sensations during wakefulness. When amputated patients dream, however, the phantom limb may be present all the time, part of the time, intermittently or not at all.¹ The absence of the phantom limb when dreaming has been taken as evidence for a pre-existing kinesthetic body scheme, unaffected by the amputation, that is accessible to the patient when asleep.² Such dreaming experiences in amputees have usually been obtained only retrospectively in the morning and, moreover, dreaming is normally associated with muscular atonia so the motor counterpart of the phantom limb experience cannot be observed directly. REM sleep behaviour disorder (RBD), in which muscle atonia is absent during REM sleep and patients act out their dreams,³ allows a more direct analysis of the “phantom limb” phenomena and their modifications during sleep.

CASE PRESENTATION

A 58-year-old man had a history of erectile failure and abnormal ejaculation, a 5 year history of orthostatic hypotension and frequent somniloquy with excessive motor activity during sleep, usually accompanied by vivid striking dreams, sometimes of violent content but not causing self- or bed-partner injury. At the age of 39 years, his left arm was amputated at the level of the middle-third of the humeral diaphysis, after it was crushed under a press. After the amputation, he experienced bothersome phantom sensations consisting of spasms and tingling or a burn-like pain in the missing hand and fingers (fig 1A). The patient could still voluntarily abduct, adduct, elevate and move the stump backwards, and could mentally execute some movements of the missing forearm, hand and fingers. Tests of cardiovascular autonomic function were consistent with central autonomic failure, and MRI by diffusion tensor imaging showed a reduction in fractional anisotropy in the cerebellum, findings consistent with possible multiple system atrophy.

Figure 1. (A) Schematic drawing by the patient of his amputated left arm (I) compared with the phantom limb experienced during wakefulness (II), and his normal body image without the phantom limb as experienced in his dreams (III).

(B) Polysomnographic recordings during REM sleep behaviour disorder showing the fast EEG activity and rapid eye movements typical of REM sleep concurrent with the absence of chin muscle atonia (mylohyoideus) and bursts of EMG activity in integer limb muscles (right wrist extensor, right and left tibialis anterior), and amputated left arm (stump EMG). ECG, electrocardiogram; EOG, electro-oculogram; L, left; R, right; SaO₂, oxygen saturation.

A diagnostic all-night videopolysomnography (VPSG) showed poor and fragmented sleep and periodic Cheyne–Stokes breathing. REM sleep was characterised by excessive increase in chin EMG tone with excessive chin and limb muscle twitches and jerks, consistent with RBD (fig 1B). Continuous movements of the left limb stump were noted during REM sleep, associated with complex, seemingly purposeful, motor activities of other limbs.

Since in the morning the patient reported that he always had a normal left arm in his dreams, and never had phantom sensations, a second VPSG was done to evaluate the content of his dreams in relation to the amputated limb. He was awakened during two successive RBD episodes, and was asked to report his dreams. The first time he reported a dream that he had recurrently, in which he was driving a car “with a very special body”, a Ferrari Testarossa, speeding, passing other cars and changing gears (he had been fond of car racing before the amputation). He reported that the amputated left arm was present and functional during the dream and that he experienced no unpleasant phantom sensations (fig 1A). When awakened during the second episode of RBD, he again reported the absence of unpleasant phantom limb sensations and confirmed the anatomical and functional integrity of his left arm in a dream in which he poured a drink for his friends while holding a bottle of champagne in his right hand and a glass in his left hand. During both episodes, his awareness of the movements of his left arm was the same as before the amputation.

DISCUSSION

This patient with an amputated limb with RBD, who had unpleasant phantom limb sensations when awake, reported the disappearance of the bothersome sensations and the recovery of the anatomical and functional integrity of the amputated limb, including motor awareness, while dreaming. Other reports of the disappearance of phantom limb phenomena during dreaming were based on subjective and retrospective (usually months later) verbal descriptions in which the original dream was reconstructed. In our patient, the description of the dream was obtained immediately, by waking the patient up in the course of REM sleep. Because of his RBD, the movements of the patient’s stump and other limbs could also be monitored by video and EMG while he was dreaming, and seemed to be congruent with the content of the dream.

Provided that the description accurately reflected the dream, our observation shows that the patient still maintained a sensor–motor representation of his limb before amputation that was accessible to awareness during sleep and responded “normally” to motor control. We cannot argue whether this body scheme was innate or established by previous, probably early life, sensory and motor experiences.² It is however of interest that behaviours acquired late in life, like driving a car or pouring from a bottle, were incorporated into the normal body scheme while dreaming.

The relevant point is however the fact that representation of the limb accessed during REM sleep was not affected by the limb amputation. We suggest that the reason why the patient had unpleasant “phantom limb experiences” while awake but not asleep, may have to do with maintenance of a normal body image conflicting with afferent information about the amputated limb. If this hypothesis of ours is true (ie, that the unpleasant “phantom limb” arises from afferent information about the amputated limb (sensitive afferences from the stump, visual expectancy, etc) harping against the fixed body image) it follows that the “phantom” limb disappears while dreaming because the complex sensory information that permits experience of the limb as it is, is blocked during REM sleep, a state during which consciousness is turned toward the inner body not the external world.⁴ Thus the unpleasant “phantom” experiences during wakefulness, resulting from a discrepancy between a pre-existing body scheme and the actual sensory information about the missing limb, were suppressed in our patient in favour of the image of the intact body accessed by default during dreaming. Our observations are in agreement with neurophysiological investigations on “phantom limb” that demonstrate the persistence of sensory–motor representations of the missing limb in the cortex.⁵ While however we cannot directly derive the brain structures (whether cortex, thalamus, brainstem, etc) where inhibition of sensory–motor information about the missing limb results in suppression of the unpleasant “phantom limb” phenomena, our clinical observation indicates that they must be neural structures that are inhibited during REM sleep.

LEARNING POINTS

• Limb amputation is followed, in approximately 90% of patients, by “phantom limb” sensations during wakefulness.

• Phantom limb sensations disappear during sleep.

• In the case described here, the dreams of a man with a phantom limb while awake are described.