Misidentification Syndromes Related to Face Specific Area in the Fusiform Gyrus

Home , Fusiform face area, Fusiform gyrus, Parahippocampal gyrus

J Neurol Neurosurg Psychiatry 2000;69:645–648 645 J Neurol Neurosurg Psychiatry: first published as 10.1136/jnnp.69.5.645 on 1 November 2000. Downloaded from

SHORT REPORT

Misidentiﬁcation syndromes related to face speciﬁc area in the fusiform gyrus

Arthur J Hudson, Gloria M Grace

Abstract consistently misidentifies a familiar place, The “delusional misidentification syn- sometimes including occupants, as a replica. dromes” are a group of uncommon and Twenty years later a more common but similar varied disorders in which, in typical form, phenomenon involving people, called the patient thinks that a particular famil- “l’illusion des sosies” or Capgras syndrome,2 iar person is someone else or a certain was described wherein an usually familiar per- familiar place is a duplicate. Although son, such as a family member, is viewed as a first identified and considered a memory stranger with an identical appearance. Since disorder by Pick, evidence in support of then, similar variants have been reported, this has been diYcult to identify. They including the Frégoli syndrome in which, as in have been most often seen in various psy- the case described in this account, the patient chotic and organic brain diseases but conceptually misidentifies a person as another lesions have been generally diVuse al- known person with an entirely diVerent though the right temporal lobe has been appearance.3 The cause of these delusional implicated. A patient was investigated misidentification syndromes, as they are collec- who abruptly developed a disorder tively known,4 is obscure although Pick1 main- copyright. wherein she misidentified her husband as tained that the phenomenon represented a dis- her deceased sister and claimed that her turbance of memory, specifically involving “a home was a duplicate of her real home sense of familiarity”, that plays “an important that were typical of Frégoli syndrome and part in remembrance, especially in recogni- Pick’s reduplicative paramnesia, respec- tion”. tively. A discrete area of brain damage, Although often described in relation to psy- probably ischaemic, in this patient was chotic states including schizophrenia, it is, seen on MRI in the anterior part of the nevertheless, widely considered that these syn- right fusiform gyrus and a smaller area in dromes have an anatomical basis because of the nearby anterior middle and inferior their frequent association with organic brain temporal gyri with associated parahip- disease.45 Brain lesions generally have been pocampal and hippocampal atrophy. A http://jnnp.bmj.com/ poorly localised and are often bilateral al- high order nervous system function that is though lesions in the right temporal lobe have devoted to the identification of faces is 5 6 located in the adjacent midportion of the been described. Sellal et al described both fusiform gyrus and a similar locus for Capgras syndrome and delusional misidentifi- environmental scenes, termed the para- cation for place in a case of viral encephalitis hippocampal place area, is present in the with damage to the anterior medial part of the bordering parahippocampal gyrus. The right temporal lobe and the medial frontal and

misidentification phenomena in this case orbital frontal regions bilaterally. Hirstein and on September 25, 2021 by guest. Protected 7 can be explained by disruption of the con- Ramachandran postulated that Capgras syn- nections of these highly specialised areas drome could be explained by damage to Department of Clinical connections from face processing areas in the Neurological Sciences, with the most anterior inferior and medial London Health part of the right temporal lobe where long right temporal lobe to the limbic system. Sciences Centre term memory and mechanisms for the Hence, our finding of discrete lesions in the (University Campus), retrieval of information that are required right anterior inferior temporal lobe has 339 Windermere Road, for the visual recognition of faces and provided a rare opportunity to confirm the London, Ontario, N6A scenes are stored. suspected organic basis and anatomical locali- 5A5, Canada (J Neurol Neurosurg Psychiatry 2000;69:645–648) A J Hudson sation for these kinds of delusions. The visual G M Grace phenomenon in these disorders is distinct from Keywords: fusiform gyrus face area; parahippocampal prosopagnosia in which familiar faces are place area; delusional misidentification; Frégoli syn- Correspondence to: perceived but not recognised. None the less, Dr A J Hudson drome [email protected] pure prosopagnosia is associated with damage to nearby right temporal cortical areas that Received 24 November 1999 Pick,1 almost a century ago, described a include, predominantly, the lingual and poste- and in final form 5 June 2000 syndrome that he named “reduplicative param- rior half of the fusiform and parahippocampal Accepted 6 June 2000 nesia” in which a person repeatedly and gyri.89

www.jnnp.com 646 Hudson, Grace J Neurol Neurosurg Psychiatry: first published as 10.1136/jnnp.69.5.645 on 1 November 2000. Downloaded from copyright. http://jnnp.bmj.com/

MRI of the patient’s brain. (A) A coronal T2 weighted image through the temporal lobe at the level of the hippocampus shows abnormal hyperintensity in the right middle and inferior temporal gyrus (small arrow in all ﬁgures) and fusiform gyrus (large arrow in all ﬁgures). (B) Proton density image of the same area as shown in A, illustrates enlargement of the right temporal horn (divided by cut into two sections as in C). There are also atrophic changes in the right hippocampus and parahippocampal gyrus and (not shown) in the fusiform gyrus. (C) Axial FLAIR image through the temporal lobe at the level of the inferior tip of the temporal horn shows the anteroposterior extent of hyperintensity in the right inferior temporal and fusiform gyri. (D) Schematic illustration of the inferior surface of the brain demonstrates the approximate on September 25, 2021 by guest. Protected extent of the damage (grey shade) in the fusiform gyrus as derived from the MRI in comparison with the putative location and extent of the fusiform face (hatched) area.14 CS=collateral sulcus; FG=fusiform gyrus; ITG=inferior temporal gyrus; LG=lingual gyrus; OTS=occipitotemporal sulcus; PG=parahippocampal gyrus.

Case report address him by the sister’s name and would The subject, a 71 year old woman, began hav- become argumentative and hostile towards him ing frequent fainting attacks from intermittent as though he were intruding. Intermittently she complete heart block. This was confirmed would speak to him using his real name, when an electrocardiographic tracing obtained expressing their usual intimacy and clearly at during an episode of unconsciousness dis- such time recognising him as her husband. In closed an abrupt drop in her heart rate from 72 this context it is noteworthy that visual contact to 30 beats per minutes for 10 seconds. Within seemed necessary for misidentification in as a day or two of the recording she was given a much as she never misidentified him as her sis- permanent cardiac pacemaker with immediate ter on the telephone. In addition to misidenti- and complete arrest of fainting. However, dur- fying him she often referred to their home as a ing the first few days of the attacks, she began rented replica and would even pack her bags to misidentifying her husband as her elder sister return to their “real” home. Sometimes she who had died 3 years previously. She would thought other members of her family, all of

www.jnnp.com Misidentiﬁcation syndromes related to face speciﬁc area in the fusiform gyrus 647 J Neurol Neurosurg Psychiatry: first published as 10.1136/jnnp.69.5.645 on 1 November 2000. Downloaded from

Table 1 Neuropsychological tests temporal lobe (figure). There was also atrophy of the right parahippocampal and hippocampal Classification range* gyri. Normal (average) Subnormal (impaired) Performance on neuropsychological testing (table), about 1 year after the onset of the syn- Test High to mid Low Mild Moderate to severe drome, was in the average to above average Wechsler adult intelligence scale-revised: range on tests of verbal intellectual skill and Verbal IQ + reasoning, most language functions, mental Subset scores Information + calculation, auditory attention, and concentra- Digit span + tion (digit span), oral and manual praxis, and Vocabulary + many aspects of verbal learning and memory. Arithmetic + Comprehension + However, there were deficits in visual percep- Similarities + tion and construction and her performance IQ Performance IQ + was significantly lower (25 points) than verbal Subset scores: Picture completion + IQ. Deficits were apparent in visual attention Picture arrangement + (visual span), memory for visual material Block design + (visual reproduction), and visual motor Object assembly + Digit symbol + processing speed (trail making test). Executive Wisconsin card sorting test:† processes such as word generation (semantic Number of categories + Perseverative responses + fluency) and organisational memory (Rey Non-perseverative responses + auditory verbal learning test) were mildly to Trail making test: moderately impaired, and several qualitative Part A + Part B + impairments of executive function were noted. Wide range achievement test - 3: For example, on delayed recall of the Rey com- Reading subtest + plex figure, perseveration was illustrated when Multilingual aphasia examination: Benton visual naming + her drawing resembled not the appropriate fig- Controlled oral word association: + ure but one drawn much earlier in the testing. Semantic fluency test (animals) + Recognition of persons with whom she had Wechsler memory scale-revised: Logical stories I + fairly regular, but not intimate, contact and Logical stories II + pictures of famous faces and places were mark- Paired associate I + edly impaired when compared with control Paired associates II + Visual reproduction I + subjects although none was misidentified. By Visual reproduction II + contrast, her identification of the faces of fam- Visual span + copyright. Rey auditory verbal learning test:† ily members in old or relatively recent photo- Total words over 5 trials + graphs, including those of herself, all siblings List B (words recalled) + and her husband, was generally accurate, a dis- Immediate recall list A + Delayed recall list A + parity that is also seen in some cases of 8 Delayed recognition + prosopagnosia. Moreover, she recognised her- Rey Osterrieth complex figure:† self in a mirror, and emotions displayed in Copy + Delay + photographs of faces were correctly inter- Clock drawing:†‡ + preted. From a psychological perspective, misi- Oral and manual praxis screening‡ + dentification of her husband as her sister and Grooved pegboard test: Right hand + her home as a replica were alike in as much as Left hand + they involved memory of familiar persons or Geriatric depression scale (items endorsed) + scenes. Both types of delusions had in common http://jnnp.bmj.com/ *Classification range based on age and/or education corrected normative data. the recall of specific remote memories of famil- †Qualitative evidence for perseveration and other executive dysfunction on these tests. iar persons or scenes that were evoked by visual ‡Evaluated qualitatively. contact with other familiar persons or scenes. whom were either deceased or at the time living elsewhere, were occupying their house although when asked she could not locate them. Discussion Despite these relentless delusions, which were The recent discovery of a face specific area in

10 11 on September 25, 2021 by guest. Protected unchanged 2 years later, the patient was alert the fusiform gyrus and a similar parahippocampal place area12 13 within the same region and cooperative and even openly discussed as the damage in the anterior fusiform gyrus in these experiences although insisting they were this patient, has provided an opportunity to real. She seemed aware of her current sur- anatomically localise and consider how the roundings during tests in hospital with no out- visual misidentification syndromes were ward indication of thought disorders or other caused. The fusiform face area is located in the neurological abnormality. Speech was fluent midportion of the right fusiform gyrus and, as and articulate, and aVect and behaviour were shown in the figure, D, lies immediately poste- appropriate. Epilepsy was excluded with three rior to the damaged region.14 Thus, to relate the independent EEGs that showed no evidence of Frégoli syndrome to the lesion in the anterior seizure activity and the delusional phenomena fusiform gyrus, it may be assumed that there were not relieved by anticonvulsant medica- has been interference with specific past visual tions. Brain MRI, performed 3 months after memories causing impaired associations of onset of delusions, showed damage, probably human faces. Some possible anatomical con- ischaemic in origin, to the anterior half of the nections of the fusiform face and parahippoc- right fusiform gyrus and a smaller area in the ampal place areas involving visual memory nearby middle and inferior gyri of the right recall can be considered.

www.jnnp.com 648 Hudson, Grace J Neurol Neurosurg Psychiatry: first published as 10.1136/jnnp.69.5.645 on 1 November 2000. Downloaded from

Sergent et al,15 using PET in face recognition interpreted as “delusions”, requires further tasks, found activation in the fusiform gyrus knowledge of mnemonic processes. and the most anterior inferior part of the temporal lobe, including the temporal pole and the We are grateful to Dr Donald Lee, Department of Diagnostic adjacent medial areas of both hemispheres. Radiology, Professor John A Kiernan, Department of Anatomy, The right parahippocampal gyrus also showed and Professor Tutis Vilis, Department of Physiology, University of Western Ontario, for their helpful suggestions in preparation increased activity. The anterior inferior tempo- of the manuscript. ral cortex has been described by Miyashita et al16–19 as the storehouse of long term visual 1 Pick A. Clinical studies. Brain 1903;26:242–67. memory where there are mechanisms for the 2 Capgras J, Reboul-Lachaux J. L’illusion des “sosies” dans retrieval and association of visually related un délire systématisé chronique. Bulletin de la Société Clinique Médécine Mentale 1923;2:6–16. information from the posterior cerebral corti- 3 Courbon P, Fail G. Syndrome d’ “illusion de Frégoli” et ces for the purpose of visual identification. schizophrénie. Bulletin de la Société Clinique Médécine Men- tale 1927;15:121–5. Face recognition properties in the fusiform 4 Marková IS, Berrios GE. Delusional misidentifications: gyrus are considered to be among such facts and fancies. Psychopathology 1994;27:136–43. 5 Feinberg TE, Shapiro RM. Misidentification: reduplication memory related associative functions of the and the right hemisphere. 18 Neuropsychiatry Neuropsychol anterior inferior temporal region. However, Behav Neurol 1989;2:39–48. 6 Sellal F, Fontaine SF, Van Der Linden M, et al.Tobeornot the selection and retrieval of visual memory to be at home? A neuropsychological approach to delusion from this region, such as required for the for place. J Clin Exp Neuropsychol 1996;18:234–48. 7 Hirstein W, Ramachandran VS. Capgras syndrome: a novel recognition of human faces and scenes, is probe for understanding the neural representation of the under the executive control of the prefrontal identity and familiarity of persons. Proc R Soc Lond B 1997; 17 19 20 264:437–44. cortex. Visual information encoded in, 8 Damasio AR, Tranel D, Damasio H. Face agnosia and the and retrieved from, long term memory also neural substrates of memory. Annu Rev Neurosci 1990;13: requires the participation of the parahippoc- 89–109. 9 Tranel D. Higher brain functions. In: Conn PM, ed. Neuro- ampal cortex, which has a pivotal memory science in medicine. Philadelphia: J B Lippincott, 1995:555– function relaying information between the hip- 80. 10 McCarthy G, Puce A, Gore JC, et al. Face-specific process- pocampus and cortex, including both the sen- ing in the human fusiform gyrus. J Cogn Neurosci sory association and prefrontal cortices.12 18 20–22 1997;9:605–10. 11 Kanwisher N, McDermott J, Chun MM. The fusiform face Thus, the parahippocampal cortex may pro- area: a module in human extrastriate cortex specialized for vide the means whereby stored memories, face perception. J Neurosci 1997;17:4302–11. 12 Tong F, Nakayama K, Vaughan JT, et al. Binocular rivalry when related to current perceptions, are and visual awareness in human extrastriate cortex. Neuron retrieved.18 23 1998;21:753–9. 13 Epstein R, Kanwisher N. A cortical representation of the The lesion in the right fusiform gyrus in this local visual environment. Nature 1998;392:598–601. copyright. case extended from the face specific area in the 14 Tovée MJ. What are faces for? Curr Biol 1995;5:480–2. 15 Sergent J, Ohta S, Macdonald B. Functional neuroanatomy middle of the gyrus to within a short distance of face and object processing. A positron emission tomog- from the tip of the temporal pole (figure, C and raphy study. Brain 1992;115:15–36. 16 Naya Y, Sakai K, Miyashita Y. Activity of primate D). Consequently, the Frégoli syndrome is inferotemporal neurons related to a sought target in explained by damage having occurred to pair-association task. Proc Natl Acad Sci USA 1996:93: 2664–9. connections within the anterior fusiform gyrus 17 Tomita H, Ohbayashi M, Nakahara K, et al. Top-down sig- that extend between the fusiform face area and nal from prefrontal cortex in executive control of memory retrieval. Nature 1999;401:699–703. the anterior inferior temporal association 18 Sakai K, Miyashita Y. Memory and imagery in the temporal cortex on which appropriate retrieval of long lobe. Curr Opin Neurobiol 1993;3:166–70. 10 19 Hasegawa I, Fukushima T, Ihara T, et al. Callosal window term memory of faces would depend. Simi- between prefrontal cortices: cognitive interaction to larly, impairment of connections of the para- retrieve long-term memory. Science 1998;281:814–18.

20 Brewer JB, Zhao Z, Desmond JE, et al. Making memories: http://jnnp.bmj.com/ hippocampal place speciﬁc area with the ante- brain activity that predicts how well visual experience will rior inferior temporal cortex can account for be remembered. Science 1998;281:1185–7. 21 Van Hoesen GW. The parahippocampal gyrus. New the phenomenon in which the patient inter- observations regarding its cortical connections in the mon- preted her house as a replica.13 21 24 As found on key. Trends Neurosci 1982;5:345–50. 22 Horton JC. The central visual pathways. In: Hart WM Jr, psychological testing, prefrontal executive con- ed. Adler’s physiology of the eye. St Louis: Mosby Year Book, trol of memory may also have been aVected 1992:728–72. 23 Goldman-Rakic PS, Selemon LD, Schwartz ML. Dual through injury to connections with the para- pathways connecting the dorsolateral prefrontal cortex hippocampal gyrus. However, a physiological with the hippocampal formation and parahippocampal

cortex in the rhesus monkey. Neuroscience 1984;12:719–43. on September 25, 2021 by guest. Protected explanation for the substitutive recall of remote 24 Teng E, Squire LR. Memory for places learned long ago is visual memories in place of current experience, intact after hippocampal damage. Nature 1999;400:675–7.