Journal of Neuro-Ophthalmology, March 1999, Volume 19, Issue 1

Visual Environmental Rotation

A 70-year-old man experienced an unusual disorder of visual perception after undergoing a ventriculoperitoneal shunt for normal-pressure hydrocephalus. The disorder was characterized by transient episodes of 90 degrees rotation of the visual environment, rather than the retinotopic visual field. This phenomenon is different from standard visual allesthesia and may have been caused by disordered integration of vestibular and visual inputs to the posterior parietal cortex or perseveration of a pre-existing environmental memory trace.

Journal of Nemo- Ophthalmology 19( 1): 13- 16, 1999. © 1999 Lippincoll Williams & Wilkins, Inc., Philadelphia Visual Environmental Rotation: A Novel Disorder of Visiospatial Integration Christopher A. Girkin, M. D., Julian D. Perry, M. D., and Neil R. Miller, M. D. A 70- year- old man experienced an unusual disorder of visual perception alter undergoing a ventriculoperitoneal shunt for normal- pressure hydrocephalus. The disorder was character­ized by transient episodes of 90° rotation of the visual envi­ronment, rather than the retinotopie visual field. This phenom­enon is different from standard visual allesthesia and may have been caused by disordered integration of vestibular and visual inputs to the posterior parietal cortex or perseveration of a pre- existing environmental memory trace. Key Words: Craniotopic- Environmental rotation- Hydro­cephalus- Posterior parietal cortex- Retinotopie- Ventriculo­peritoneal shunt- Visual allesthesia. Visual allesthesia is a rare disorder of visual percep­tion characterized by rotation or transposition of the vi­sual field ( 1). We report a patient who experienced tran­sient episodes of 90° rotation of the visual environment, rather than the retinotopie visual field, after placement of a ventriculoperitoneal ( VP) shunt through the right pari­etooccipital cortex. CASE REPORT A 70- year- old man with a medical history of con­trolled hypertension had a 2- year history of gradually increasing gait impairment. Magnetic resonance imaging revealed marked ventricular enlargement suggestive of communicating hydrocephalus, and he was referred to the Neurosurgical Service of the Johns Hopkins Hospital for evaluation. The patient underwent diagnostic lumbar catheterization with cerebrospinal fluid ( CSF) pressure monitoring and controlled CSF drainage. His gait distur­bance improved after the procedure, and he elected to undergo placement of a VP shunt. A VP shunt was placed on August 1, 1997, through the right parieto- occipital cortex, after which the patient's gait markedly improved. However, on the first postop­erative day, the patient began to experience episodes of Manuscript received February 5, 1998; accepted July 8, 1998. From the Neuro- Ophthalmology Unit, The Johns Hopkins Medical Institute, Baltimore, Maryland, U. S. A. Address correspondence and reprint requests to Neil R. Miller, M. D., Maumenec B- 109, The Johns Hopkins Hospital, 600 N Wolfe Street, Baltimore, MD 21287, U. S. A. transient static rotation of his visual environment that lasted from 10 to 20 minutes. He described each episode as " feeling like I'm walking on the wall." The visual environment appeared rotated 90° around a coronal axis. When the patient looked forward while sitting, the ceil­ing appeared in front of him, and the wall he was facing appeared underneath him. The side walls appeared to be rotated 90° clockwise. When he looked to either side, the rotational axis did not change with the new head posi­tion. Thus, when he looked at a side wall, it did not appear underneath him; rather, it remained rotated 90° clockwise, as it had appeared when he was looking straight ahead ( Fig. 1, bottom left and bottom right). This illusion was not associated with dizziness, and it abated when he closed his eyes. These episodes occurred three to six times a day, re­solving by the sixth day after surgery. Neurologic and neuro- ophthalmologic examinations were unremarkable other than for a mild gait disturbance. The patient had received no pain medications after surgery, and his men­tal status was normal. Computed tomographic ( CT) scanning 3 clays after surgery revealed good catheter placement through the right parieto- occipital cortex with minimal blood in the right occipital horn and no other abnormalities ( Fig. 2). During his CT scan, the patient had an episode of envi­ronmental rotation that lasted for the duration of the scan. He described the sensation of entering the scanner as being moved " vertically up into the tube." An electroencephalogram ( EEG) was obtained 1 week after surgery and was normal. However, the episodes had stopped before the EEG was performed. The patient has had no further episodes since his hospitalization. DISCUSSION Classic visual allesthesia is a disorder of visiospatial perception in which the retinotopie visual field is rotated, flipped, or inverted ( 2). Visual allesthesia may be a manifestation of parieto- occipital or occipital lobe dis­ease caused by neoplasm, infection, trauma, or seizure activity ( 3- 6). This phenomenon may also occur with multiple sclerosis ( 7) and migraine ( 8). Visual allesthesia may also occur in patients with lateral medullary infarc- 13 14 C. A. G1RK1N ET AL. FIG. 1. Illustrations on the left show the view and orientation when the subject is looking forward. Illustrations on the right show the view and orientation looking to the left. Upper left and upper right figures show a third- person view of the patient's room, indicating the head position and the orientation of the environment that would be seen by a normal person looking forward ( left) and to the left ( right). Center left and center right figures illustrate the appearance of the environment that would be seen by a patient with classic visual allesthesia looking forward ( center left) and to the left ( center right). Note that there is transposition of the visual field. Lower left and lower right figures illustrate the environmental rotation experienced by our patient. Note that, in contrast to the rotation seen by a patient with classic visual allesthesia, the rotation is independent of head position. ./ Ncitro- Ophlhalmol, Vol. 19, No. I, 1999 VISUAL ENVIRONMENTAL ROTATION 15 FIG. 2. Unenhanced computed tomographic scan, axial view, shows the ventriculoperitoneal catheter { arrowhead} traversing the right parieto- occipital cortex. There is minimal blood in the occipital horn of the right lateral ventricle. tion, but it is related to a disturbance in otolith inputs at the level of the brainstem and not to a higher cortical disorder in such cases ( 9). Several theories have been proposed to explain visual allesthesia; however, an all- encompassing explanation remains elusive. Jacobs ( 10) suggested that allesthesia may involve transcallosal transmission of images from the contralateral hemifield to the damaged parietal cor­tex, with retention of the images as a palinopsic phenom­enon. Some cases may thus represent a perseveration of visual perceptions similar to the visual experiences that occur during electrical stimulation of the cerebral cortex in conscious humans ( 11). Although this theory may ex­plain the patient Jacobs described who had transposition of the visual field from left to right, it fails to explain the varieties of rotational or inverted allesthesia reported by other patients. Alternately, visual allesthesia may be caused by a dis­order of integration of visiospatial input. The causative lesions may disturb the integration of visual and otolithic inputs, either directly at the level of the medulla ( as in Wallenberg's syndrome) or indirectly at the site of inte­gration in the posterior parietal cortex, thus causing tilt­ing or inversion of the visual field ( 12). In contrast to classic visual allesthesia in which the visual field is rotated, our patient's visiospatial illusion involved a static rotation of the visual environment. The right occipitoparietal cortex, through which the shunt was placed, is thought to play a major role in modulating the internal representation of external space ( 13) and when lesioned may produce a variety of visiospatial dis­orders, such as visual allesthesia and palinopsia. Numerous physiologic experiments have shown that the posterior parietal cortex contains multiple abstract representations of external space interposed between sensory input and motor output ( 13). Visual information, head- position coordinates conveyed by otolithic inputs, and eye- position coordinates are combined to create an internal representation of external space that records the location of visual objects in oculocentric ( 14), craniocen-tric ( 15), and possibly even a world- centered coordinate system ( 16). Galletti et al. ( 15) reported the existence of " real-position" cells in the parietal cortex, mostly limited to area V6, of two Macaco monkeys. The receptive fields of these cells did not vary with gaze and responded to visual stimulation from the same spatial location regard­less of eye position. They thus encoded visual space in a craniotopic coordinate system ( i. e., real- position). A dis­order involving this real- position system, related to irri­tation from the ventricular shunt, could thus have caused the transient illusions of environmental rotation, inde­pendent of head and body position, perceived by our patient. In our patient, the visual environment was ro­tated, not the visual field. This indicates a disturbance in the craniotopic visual precept rather than in the retino-topic visual field that occurs in classic allesthesia. Thus, the illusion in this case may be secondary to disordered integration of vestibular and visual inputs to the posterior parietal cortex causing misalignment of the visual envi­ronment. Alternatively, these episodes may represent persevera­tion of a pre- existing environmental memory trace. The posterior parietal lobe system forms a neural image of surrounding space constructed from visual, vestibular, and eye- position signals. Colby and Duhamel ( 16) showed that the posterior parietal cortex remaps stored visual information before a saccadic eye movement to predict the relative position of objects as they would appear after the saccade. This preemptive remapping of the stored visual environmental model in conjunction with afferents to the superior colliculus may play a role in spatial constancy. However, psychophysical experi­ments have demonstrated that this environmental remap­ping may not only affect motor behavior but also alter environmental perception ( 17). Indeed, an irritated pos­terior parietal cortex has been shown to invoke visual experience ( 2). Perhaps a previously perceived environ­mental memory trace was recalled secondary to irritation from the shunt tube in our patient, thus altering his per­ception of environmental alignment. The illusion expe­rienced by the patient may therefore represent a perse­veration of an environmental memory trace; that is, " en­vironmental palinopsia." In conclusion, we present a novel case of a visiospatial disturbance causing an illusional rotation of the visual environment that, without careful questioning, might have been assumed to be classic visual allesthesia. J Neiao- Oiilitlialmol. Vol. 19. No. I. 1999 16 C. A. GIRKIN ETAL. REFERENCES 1. Meador KJ, Allen ME, Adams RJ, Loring DW. Allochiria vs. allesthesia: is there a misperception? Arch Neurol 1991; 48: 546- 9. 2. Jacobs L. Visual allesthesia. Neurology 1980; 30: 1059- 63. 3. Erctto PA, Schoen FS, Krohel GB, Pechette D. Palinoptic visual allesthesia. Am J Ophthalmol 1982; 93: 801- 3. 4. Nakajama M, Yasue M, Kaito N, Kamikubo T, Sakai H. A case of visual allesthesia. Nolo Shinkei 1991: 43: 1081- 5. 5. Ardila A, Botcro M, Gomez J. Palinopsia and visual allesthesia. Int J Neiiro. se 1987: 32: 775- 82. 6. Bender MB. Ncuro- ophlhalmology. In: Baker AB, Baker LH, eds. Clinical neurology. Vol. 1. New York: Harper & Row, 1977: 37- 8. 7. Seigel AM. Inverted vision in multiple sclerosis. Neurology 1988; 30: 1335. 8. Hachinski VC, Porchaweka J, Steele JC. Visual symptoms in the migraine syndrome. Neurology 1973; 23: 570- 9. 9. Ropper MB. Illusion of tilting of the visual environment. Report of 5 eases. ./ Clin Neuro- ophthalmol 1983; 3: 147- 51. 10. Jacobs L. Visual allesthesia. Neurology 1979; 29: 599. 11. Penfield W, Perot P. The brain's record of auditory and visual experience. Brain 1963; 86: 595- 6. 12. Tiliket C, Ventre- Dominey J, Vighetto A, Grochowicki M. Room tilt illusion: a central otolith dysfunction. Arch Neurol 1996; 53: 1250- 64. 13. Anderson RA. Encoding of intention and spatial location in the parietal cortex. Cereb Cortex 1995; 5: 457- 69. 14. Colby CL, Duhamel J- R, Goldberg ME. Oculocentric spatial rep­resentation in the parietal cortex. Cereb Cortex 1995; 5: 470- 81. 15. Gallctti C, Battaglini PP, Fattori P. Parietal neurons encoding spa­tial locations in craniotopic visual coordinates. Exp Brain Res 1993; 96: 221- 9. 16. Colby C, Duhamel J- R. Spatial representation for action in parietal cortex. Cognitive Brain Res 1996; 5: 105- 15. 17. Hikosaka O, Miyauchi S, Shimojo S. Visual attention revealed by an illusion of motion. Neurosci Res ] 993; 18: 11- 8. ./ Neiiro- Oplilluilmoi, Vol. 19, No. I. 1999