Journal ofNeurology, Neurosurgery, and Psychiatry 1997;62:261-264

Impairment of facial recognition in patients withright cerebral infarcts quantified by computeraided "morphing"

A Rosler, S Lanquillon, 0 Dippel, H J Braune

Department ofNeurologyA RoslerH J BrauneDepartment ofPsychiatryS LanquillonInstitute ofComputerScience, PhilippsUniversity, Marburg,Germany0 DippelCorrespondence to:Dr Alexander Rosler,University HospitalMarburg, Rudolf-BultmannStrasse 8, 35033 Marburg,Germany.Received 4 March 1996and in revised form19 September 1996Accepted 30 October 1996

AbstractObjective-To investigate where facialrecognition is located anatomically and toestablish whether there is a graded transi-tion from unimpaired recognition offacesto complete prosopagnosia after infarc-tions in the territory of the middle cere-bral artery.Methods-A computerised morphingprogram was developed which shows 30frames gradually changing from portraitphotographs of unfamiliar persons tothose of well known persons. With a stan-dardised protocol, 31 patients with rightand left sided infarctions in the territoryof the middle cerebral artery and an ageand sex matched control group were com-pared by non-parametric tests.Results and conclusion-Facial recogni-tion in patients with right sided lesionswas significantly impaired compared withcontrols and with patients with left sidedlesions. A graded impairment in facialrecognition in patients with right sidedischaemic infarcts in the territory of themiddle cerebral artery seems to exist.

(7 Neurol Neurosurg Psychiatry 1997;62:261-264)

Keywords: prosopagnosia; facial recognition; stroke

It is unlikely that we are able to distinguish anyother object to such a degree as we can humanfaces. The idea that recognition of a humanface could be a function which is independentof other recognition modalities of the brain,and therefore could also be independently dis-turbed, was finally established by Bodamer in1947.' Previous to this reports of disturbancesin facial recognition had been made byWillebrand2 and Charcot.3 If we assume anisolated function of facial recognition, twosubstantial issues arise: (1) Where is it locatedanatomically? (2) Is there a graded transitionfrom unimpaired recognition of faces to com-plete prosopagnosia?

Patients and methodsTo elucidate these questions, 31 right handedpatients with ischaemic infarcts in the supplyarea of the middle cerebral artery (15 left sidedand 16 right sided infarcts) were studied andcompared with 21 age and sex matched con-trols. The distribution of Barthel indices wasthe same for left and right sided infarcts (mean= 84 and median = 90 for left and mean =84 and median = 95 for right sided infarcts).The following inclusion criteria were applied:cranial CT confirmed a single infarction in thesupply area of the middle cerebral artery (table1 shows the topographical distribution); no. .

:#:.. _.:

w__ r.>s#._ _.:E ^:

rx. .... 4.........wr:oF

.:S' '-°At i

*': ' S,9tt

'. .g; r

*;l' tdjle;j3 [';b Ctfe

[.: .e

i;;'0 '*tC fi, wm 0-_E. .: ^., ia ............ : i

oS tz l-tlll ' t R a1ll L -tI-;ll-pt:1110to-raph

Sijrtilnc, frln.li

Figure 1 Selection offrames illustrating the morphing process.

261

nE...

on February 28, 2020 by guest. P

rotected by copyright.http://jnnp.bm

j.com/

J Neurol N

eurosurg Psychiatry: first published as 10.1136/jnnp.62.3.261 on 1 M

arch 1997. Dow

nloaded from

Rosler, Lanquillon, Braune, Dippel

Table I Distribution of infarcts by CT

Regio7n Right inifarcts Left infarcts

Cortical:Temporo-occipital 4 3Temporoparieto-occipital 5 4Frontotemporoparietal 1 2

Subcortical:Thalamus and internal capsule 4 3Basal ganglia 2 3

Table 2 Results with frame Diana

Attenmpts

s< 25 26-30 Failed

Controls** 16 (76 2) 2 (9-5) 3 (14 3)Left infarcts 6 (40) 4 (26-7) 5 (33-3)Right infarcts** 3 (18-8) 6 (37-5) 7 (43-8)

Percentages are in parentheses.**P = 0-002.

Table 3 Results with frame Kohl

Attemipts< 24 25-30 Failed

Controls** 16 (76 2) 5 (23-8) 0 (0)Left infarctst 9 (60) 6 (40) 0 (0)Right infarcts**t 5 (31-2) 7 (43-8) 4 (25)

Percentages are in parentheses.tP = 0 034; **p = 0-004.

Table 4 Effect of cortical and subcortical lesions on results with frame Diana

Attempts

< 25 26-30 Failed

Cortical:Left infarcts* 3 2 4Right infarcts* 0 5 5

Subcortical:Left infarcts 3 2 1Right infarcts 3 1 2

*P = 0-06 (NS).

Table 5 Effect of cortical and subcortical lesions on results with frame Kohl

Attempts

< 24 25-30 Failed

Cortical:Left infarcts** 5 4 0Right infarcts** 0 6 4

Subcortical:Left infarcts 4 2 0Right infarcts 5 1 0

**P = 0-001.

Table 6 Effect of cortical brain region involved in right sided infarcts with frame Diana

Attemipts< 25 26-30 Failed

Temporoparieto-occipital 0 1 4Temporo-occipital 0 3 1

Figure 2 Group comparisons of attempts to identifyDiana.

previous or multiple infarcts; tests were donein the second week after the stroke; exclusionof patients with moderate or severe dementiaby mini mental status examination4; andexclusion of patients with receptive aphasia bythe Aachener aphasia test.5

Each patient was shown two series of 30pictures on a video screen (fig 1). In the firstseries a photo of Jil Sander turned into a por-

trait of Lady Diana; in the second MichaelDouglas was transformed into Helmut Kohl.Patients were given 30 seconds with eachframe to recognise Lady Diana and HelmutKohl. The number of frames needed to iden-tify the target either by name or social functionwas counted. Characteristics which could haveaided in the recognition of the prominent per-

son-for example, hair, glasses, or a tie were

not shown in the photo.Based on the results of the controls for both

series of pictures, categories were developedfor normal, late, and non-identification.Seventy five per cent of the controls recog-nised Diana within 25 and Kohl within 24attempts; therefore these numbers were set as

arbitrary upper boundaries for "normal"recognition. More attempts up to the endpoint of 30 were considered "late" and no

identification at all as "failed". Patients or

controls who did not know the target persons

even after being told their names, were

excluded from analysis. Results were analysedby maximum likelihood X2 tests.67

ResultsHealthy controls recognised Helmut Kohlearly in 16 out of 21 cases and late in theremaining five. Diana was recognised early in16, late in two, and not at all in three cases.

Patients with left sided infarcts recognisedDiana and Kohl later than controls but thiswas not significant (P = 0-086 for Diana; P =

0-58 for Kohl).Patients with right sided infarcts identified

Diana and Kohl significantly later than thecontrols (P = 0-002 for Diana and P = 0 004for Kohl).

Table 7 Effect of cortical brain region involved in right sided infarcts with frame Kohl

Attempts

s< 24 25-30 Failed

Temporoparieto-occipital 0 1 4Temporo-occipital 0 4 0

262 on F

ebruary 28, 2020 by guest. Protected by copyright.

http://jnnp.bmj.com

/J N

eurol Neurosurg P

sychiatry: first published as 10.1136/jnnp.62.3.261 on 1 March 1997. D

ownloaded from

Impairment offacial recognition in patients with right cerebral infarcts quantified by computer aided "morphing"

Figure 3 Groupcomparisons of attempts toidentify Kohl.

100

80

60

40

20

.-wullullIz

Z;2-

.E<24

</ 25-30

) Far'Vi. F S

6S. S s^s_

ii ..--_

.. '_stI,)fS.ed Control

Infarcts lefttircts right. -tIs -.

Group comparisons between left and rightsided infarcts for Diana did not differ signifi-cantly (P = 0-42), whereas patients with rightsided infarcts identified Kohl significantly laterthan those with left sided infarcts (P = 0 034)(tables 2 and 3, figs 2 and 3).

Subanalysis of cortical involvement by CTshowed significant impairment of facial recog-nition in patients with right sided infarcts forKohl (P = 0-001) and did not reach signifi-cance for Diana (P = 0-06), whereas isolatedsubcortical lesions did not have a significanteffect on the recognition task (tables 4 and 5).

Involvement of the parietal lobe in rightsided lesions was associated with more recog-nition failures compared with temporo-occipitallesions alone (tables 6 and 7). No statisticalanalysis was carried out because of the fewpatients in these subgroups.

DiscussionOur patients with right sided infarcts seemedto have more difficulties in identifiying familiarfaces than healthy controls and patients withleft sided infarctions.The neuroanatomical localisation of facial

recognition and its disturbances still remaincontroversial. Kolb and Wishaw postulatedthat the damage which leads to prosopagnosiamust be bilateral. Brodman's areas 18 and 19,and additionally 20, 21, and 37 seem to play a

part in facial recognition.8 Kandel too arguedthat "lesions that cause prosopagnosia are

always bilateral".9 In a comprehensive articleby Meadows'0 there were seven postmortemresults available from patients who had hadprosopagnosia. Five of these had bilateraloccipitotemporal lesions, mostly symmetric, inaccordance with the study by Damasio et al.11The two other patients had right sided occipi-totemporal lesions.Young et al reported a 51 year old woman

who showed a deficit in recognising faces andmatching photographs of facial emotionalexpression after bilateral partial amygdalo-tomy.'2On the other hand there is little doubt that

the right hemisphere plays an important partin facial recognition: Hecaen and Angeluergesmade a list of neurological signs which were

positively associated with prosopagnosia.'3

The disorder showed associated signs suchas left visual field defects in 91% of the cases,disturbances of spatial orientation, construc-tive apraxia, and neglect. This enumerationalone indicates that right sided lesions areobviously more often related to impaired facialrecognition. The high number of combina-tions with left upper quadrantanopia led to theassumption that the underlying lesion could bein the right basal occipital lobe. Millerdescribed delayed recognition of faces inpatients who had undergone right temporallobectomy.'4 In a more recent article, Evans etal reported the case of a 68 year old womanwith progressive atrophy of the right temporallobe developing progressive prosopagnosia."5In a recent review Boeri and Salmaggifavoured a right posterior lesion in what theycalled true prosopagnosia,'6 and a patientreported by Sergent and Poncet had a largeright parietotemporal lesion sparing the medialposterior temporal cortex.'7

These in part contradictory results suggestthe possibility of different forms of impairedfacial recognition.Thus Bruce and Young developed a func-

tional model of face processing which dividesfacial processing into different modalities.After a basic process of structural encoding,there should be different pathways to theanalysis of facial expression, the recognition offamiliar faces, and the matching of unfamiliarfaces. 18We know that object recognition is

processed by a ventral pathway constituted byoccipito-temporal cortices. On the other hand,visuospatial processing of the visual scene iscomprised of parieto-occipital pathways.Different modalities for the recognition offaces play a synergistic part. When healthypersons have to discriminate elementary fea-tures like colour, the prestriate cortex and inparticular the fusiform gyrus is activated.Perceptual integration takes place in the poste-rior part of the lingual gyrus and, in a thirdstep, especially important for the recognitionof faces, mainly the anterior part of the lingualgyrus and the parahippocampic gyrus are acti-vated in attributing meaning to the "per-cept". 19

Despite this well established topographicalassociation between the visual recognitionprocess and the brain region involved, there isstill no consensus on the question of lateralisa-tion of different facial recognition modalities.For instance, results of analysing emotionalfacial expression are controversial:Young et al examined 32 servicemen 40

years after they had sustained a penetratingmissile injury to the brain in the second worldwar and found that expression analysis wasselectively impaired in five patients with lefthemispheric lesions,20 although earlier this taskhad mainly been thought to be located in theright hemisphere.2' 22

Superiority of the right hemisphere was alsoclaimed for the function of visual attentionaccording to Dimmond and Heilmann.2324 Itcould therefore be argued that the impairmentof facial recognition in our patients with right

263 on F

ebruary 28, 2020 by guest. Protected by copyright.

http://jnnp.bmj.com

/J N

eurol Neurosurg P

sychiatry: first published as 10.1136/jnnp.62.3.261 on 1 March 1997. D

ownloaded from

Rosler, Lanquillon, Braune, Dippel

sided lesions might be partly due to failure ofarousing visual interest in the emotionalexpression of the face shown. However, thelateralisation of visual attention remains con-troversial: Posner showed that patients withleft or right parietal lesions were equallyimpaired in directing their attention to stimuliin both visual fields.25The studies mentioned were all carried out

on patients with relatively longstanding braindefects, whereas in our patients the interval ofone week between the event of infarction andthe morphing task was presumably too short toallow selective testing for single modalities offacial recognition. This view is supported bythe well known finding in other neuropsycho-logical syndromes for example, aphasia orapraxia-that a final distinction of differentsubforms is not usually possible in the acutephase of brain damage.

In general we may state that the complexfunction of facial recognition requires theintegrity of the right temporoparieto-occipitalregion. This anatomical region was damagedto different extents in our patients. Three offive patients with right temporoparieto-occipitallesions failed to recognise both target pictures,the remaining two of this group received lowerscores (28 for Diana and "failed" for Kohl, 28for Kohl and "failed" for Diana) than thegroup of patients with temporo-occipitalinvolvement, in which only one of fourpatients failed with Diana and all four recog-nised Kohl. Despite the small case numbers inthese subgroups, these results suggest a possiblekey role for the parietal region in facial recog-nition.

In accordance with the results of Young andTupler,2026 our patients with lesions involvingcortical regions were significantly impaired inour test of facial recognition, whereas the sixpatients with subcortical lesions only were not(tables 2 and 3).Our patients, like others with right hemi-

sphere damage, did not complain about diffi-culties recognising faces. Probably thesedeficits are easy to compensate for, becauserecognising a certain person "behind" a face indaily life is made easy by the perception of fur-ther visual and acoustic cues.27Among the tested patients with right sided

cortical infarctions there were none withprosopagnosia in a "pure" sense, althoughthere was a clear impairment in recognition offamiliar faces; graded disturbances in the senseof a "prosophypognosia" in this common neu-rological disease do seem to exist.

With the exception of the Benton-Van Allenfacial recognition test there are only experi-mental tests available for the function of facialrecognition.28

As Puschel and Zaidel showed, the Benton-Van Allen test is not able to discriminatebetween patients with damage in the left orright hemisphere.29Morphing programs with a variable number

of features are widely available for personalcomputers and enable sensitive testing forimpairment of facial recognition.

1 Bodamer J. Die Prosop-agnosie. Arch PsychiatrNervenkrankheiten 1947;179:6-53.

2 Willebrand H. Ein Fall von Seelenblindheit und Hemian-opsie mit Sectionsbefund. Deutsch Z Nervenheilk 1892;2:361-5.

3 Charcot JM. Un cas de suppression brusque et isolee de lavision mentale des signes et des objets (formes etcouleurs ). ProgrMed 1883;11:568-74.

4 Folstein MF, Folstein SE, Hugh PR. "Mini-mental-state". Apractical method for grading the cognitive state ofpatients for the clinician. Jf Psychiatr Res 1975;12: 189-98.

5 Huber W, Poeck K, Weniger D, Willmes K. Der AachenerAphasie Test. Guttingen: Holzgrefe, 1983.

6 Bishop YMM, Fienberg SE, Holland PW. Discrete multi-variate analysis. Cambridge, MA: MIT Press, 1975.

7 Fienberg SE. The analysis of cross-classified categorical data.Cambridge, MA: MIT Press, 1977.

8 Kolb B, Wishaw IQ. Fundamentals of human neuropsychol-ogy. New York: W H Freeman, 1990, 236-7.

9 Kandel ER, Schwartz JT, Jessel TM. Principles of neuro-sciences. New York: Elsevier, 1991, 458-9.

10 Meadows JC. The anatomical basis of prosopagnosia. J7Neurol Neurosurg Psychiatry 1974;37:489-50 1.

11 Damasio AR, Damasio H, Van Hoesen GW.Prosopagnosia: anatomic basis and behavioural mecha-nisms. Neurology 1982;32:33-41.

12 Young AW, Aggleton JP, Hellawell DJ, Johnson M, BrooksP, Hanley JR. Face processing impairments after amyg-dalotomy. Brain 1995;118:15-24.

13 Hecaen H, Angelergues R. Agnosia for faces (prosopag-nosia). Arch Neurol 1972;7:92-100

14 Miller B. Visual recognition and recall after right temporallobe excision in man. Neuropsychologia 1968;6:191-209.

15 Evans JJ, Heggs AJ, Antoun N, Hodges JR: Progressiveprosopagnosia associated with selective right temporallobe atrophy-a new syndrome? Brain 1995;118:1-13

16 Boeri R, Salmaggi A. Prosopagnosia. Current Opinion inNeurology 1994;7:61-4.

17 Sergent J, Poncet M. From covert to overt recognition offaces in a prosopagnosic patient. Brain 1990;113:989-1004.

18 Bruce V, Young A. Understanding face recognition. Br JfPsychol 1986;77:305-27.

19 Ceccaldi M. Visual object agnosia. Handout, teachingcourse Neuropsychology. First Congress of the EuropeanFederation of Neurological Societies Marseille: France,1995:2-4.

20 Young AW, Newcombe F, de Haan EHF, Small M, HayDC. Face perception after brain injury. Brain 1993;116:941-59.

21 Etcoff NL. Selective attention to facial identity and facialemotion. Neuropsychologia 1984;22:281-95.

22 Suberi M, McKeever WF. Differential right hemispherememory storage of emotional and non-emotional faces.Neuropsychologia 1977;15:757-68.

23 Dimmond SJ, Beaumont JG. Differences in vigilance per-formance of the right and left hemisphere. Cortex 1973;9:259-65.

24 Heilman KM, van den Abell T. Right hemisphere domi-nance for mediating cerebral activation. Neuropsychologia1979;17:315-21.

25 Posner MI, Walker JA, Friedrich JR, Rafal RD. Effects ofparietal lobe injury on covered orienting of visual atten-tion. J Neurosci 1984;4:1863-74.

26 Tupler LA, Coffey CE, Logue PE, Djang WT, FanganSM. Neuropsychological importance of subcortical whitematter hyperintensity. Arch Neurol 1992;49:1248-52.

27 Von Cramon D, Mai N, Ziegler W, eds. NeuropsychologischeDiagnostik. London: Chapman and Hall, 1995, 29-33.

28 Benton AL, Hamsher K de S, Vamey N, Spreen 0.Contributions to Neuropsychological assessment: a clinicalmanual. Oxford: Oxford University Press, 1983.

29 Puschel J, Zaidel E. The Benton-van Allen faces: a lateral-ized tachistoscopic study. Neuropsychologia 1994;32:357-67.

264 on F

ebruary 28, 2020 by guest. Protected by copyright.

http://jnnp.bmj.com

/J N

eurol Neurosurg P

sychiatry: first published as 10.1136/jnnp.62.3.261 on 1 March 1997. D

ownloaded from