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Prosopagnosia and object agnosia without covert recognition
h’ruropsycholoq~o. Vol. 27, No. 2. pp. lJ9-191, Printed in Great Bntam.
PROSOPAGNOSIA
1989.
0028-3932.89 53.00+000 c’ 1989 Pergamon Press plc
AND OBJECT AGNOSIA RECOGNITION*
WITHOUT
COVERT
FREDANEWCOMBE,?ANDREW W. YOUNG and EDWARD H. F. DE HAANt tMRC
Neuropsychology Unit, Radcliffe Infirmary, Woodstock Road, Oxford OX2 6HE, U.K.; and Psychology Department, Lancaster University, Bailrigg, Lancaster LA1 4YF, U.K. Receiced
14 March 1988; accepted
11July 1988)
Abstract-Investigations of the visual recognition abilities of the patient M.S. are reported. MS. is unable to achieve overt recognition of any familiar faces, and many everyday objects. In Task 1 he showed semantic priming from name primes but not from face primes in a name recognition task. In Task 2 he showed no advantage in learning true (face+correct name) rather than untrue (face+someone else’s name) pairings of faces and names. In Task 3 semantic priming of lexical decision was only found for object picture primes that M.S. was able to recognize overtly. In Task 4 faster matching of photographs of familiar than unfamiliar objects was only found for objects that MS. was able to recognize overtly. These findings demonstrate an absence of covert recognition effects for MS., consistent with the view that his impairment is primarily “perceptual” in nature.
INTRODUCTION
PROSOPAGNOSK patients are no longer able to recognize familiar people from their faces. The deficit can extend to even the most well-known faces including friends, family, famous people and the patient’s own face when seen in a mirror [4, 6, 10, 111. Recent studies have, however, shown that despite the almost complete breakdown of overt face recognition ability found in some cases of prosopagnosia, covert recognition may continue to take place. This covert recognition can be demonstrated in certain tasks which test recognition implicitly. BAUER [2, 31 and TRANEL and DAMASIO [ZO], for instance, demonstrated covert recognition in the form of autonomic responses to familiar faces. Similarly, DE HAAN et al. [7, S] demonstrated covert recognition using behavioural measures derived from performance in matching, learning, and interference tasks, and YOUNG et a[. [24] found semantic priming from unrecognized faces onto the recognition of name targets (for example, from seeing Princess Diana’s face to recognizing Prince Charles’s name as familiar). The existence of covert recognition allows prosopagnosia to be considered as one of a group of neuropsychological impairments characterized by what SCHACTER et al. [l S] term failures of access to consciousness. The patient’s face recognition abilities are in a sense quite well preserved, but he or she does not realize this because face recognition takes place without the normal awareness of recognition. A central issue concerns whether covert recognition is to be found for all prosopagnosic patients, or whether it only exists for a particular type of face recognition impairment. One reason for expecting the latter is that neuropsychologists interested in prosopagnosia have * This research was supported by MRC grant PC 7301443 to Freda Newcombe grant G 8519533 to Andy Young. We are grateful to the Press Association photographs of faces to use as stimuli. 179
and John Marshall, and by MRC for help in obtaining suitable
180
FREUA NEWCOMB~, ANDREW W. YOUNGand EDWARD
H. F. DE HAAN
often made a distinction between two forms of the disorder [9, 10, 121. In one form the underlying cause seems to be impairment of the highest levels of visual perception; the patients are poor at matching views of unfamiliar faces and there is usually an associated visual object agnosia [9]. In the other form of prosopagnosia ability to match views of unfamiliar faces and to recognize everyday objects is relatively intact, and the problem seems to take the form of a material-specific memory impairment (in the sense that memories concerning familiar people cannot be accessed from an adequately perceived face, yet remain accessible from other inputs, such as names or voices). Given the hypothesized existence of these perceptual and mnestic forms of prosopagnosia it is tempting to speculate that covert recognition is linked to the form involving the materialspecific memory impairment. This view would be consistent with the parallel that can be drawn between covert recognition of familiar faces in prosopagnosia and the priming and implicit memory phenomena found in cases of amnesia [17, 181. The corollary of this view is that covert recognition may not exist for the form of prosopagnosia involving the primarily perceptual impairment, an hypothesis first suggested by BAUER [3]. The present paper investigates this possibility with the patient MS., previously studied by NEWCOMBE and RATCLIFF [13] and RATCLIFF and NEWCOMBE [IS], and thought to have a higher-order perceptual impairment.
CASE DESCRIPTION MS. is a former police cadet who contracted a febrile illness in 1970, at the age of 23. The presumptive diagnosis was herpes encephalitis, but this was never confirmed by viral antibody studies. A full case description has been given by NEWCOMBEand RATCLIFF [I 31 and RAT~LIFF and NEWCOMHE[ 151, so we will only summarize the essential features of previous reports and add some new details. M.S. has a left homonymous hemianopia, but his visual acuity is normal (6/6; N5 for near vision). His colour vision is, however, severely impaired. He also has a severe object agnosia which affects his ability to recognize both real objects and object pictures. MS. can often identify a real object more readily than a picture of the same object. but his performance with both types of stimuli is ciearly defective. He was able to successfully identify only 8/36 line drawings, whereas he could name 20/36 of the same objects from verbal descriptions of their functions. He can, though, make accurate copies of drawings he has not recognized, using a line-by-line copying strategy. The fact that M .S. could only identify 20/36 objects from verbal descriptions of their functions shows that there is some impairment of semantic memory, and this IS particularly evident in tasks involving living things. Despite this, MS. remains able to read, and his performance at making “true or false”judgements about absurd sentences (46/50) is within normal limits. His readingofsingle words is accurate (94/3CO correct for regular and exception words from BAUER and STANOVICH[l]) and he can also make accurate lexical decisions (one error to the list from SAFFKANand MARIN 1161). M.S. is completely unable to recognize familiar faces. On a test involving the faces of 20 highly familiar, ?O moderately familiar, and 20 unfamiliar people he could identify no one. He was also poor at matching photographs of unfamiliar people. His score was 33/54 on the Benton Test of facial recognition (5/‘6 correct responses when matching identical views, 13/24 with changed orientation, and 15124 with changed lighting), and he only managed 49/80 correct trials in our own task of matching internal or external facial features 123; Experjment I]. This is usually given as a reaction time task, but M.S.‘s low level of performance made meaningful measurement of reaction times impractical. The mean accuracy of normal subjects when performing this task was 74.4180 correct (SD = 3.X3). MS. was also poor at matching facial expressions (25,!32 correct; normal subjects U= 29.82. SD =0.37), and relied on a strategy of comparing first the eyes rnd then the mouth (which suggests that he could not take in the appearance of the face “as a whole”). A forced-choice task was used to compare M.S.‘s ability to recognize faces and names. This task has been described in detail by YOUNGand DE HAAN1221, and consists of 128 pairs of faces and 128 pairs of names. One stimulus in each pair is a familiar person’s face or name, and one is an unfamiliar person’s face or name. The membcra of each pair of faces or names were simultaneously presented, one above the other. M.S. was asked to choose the fami!iar’member of each pair. His performance is-cbmpared with that of the prosopagnoslc patient P.H. 1221 in Table 1. MS’s performance is very similar to that of P.H. Although MS. and P.H. are both impaired for forcedchoice name familiarity decision in comparison with normal subjects, they are none-the-less highly accurate at determining whether or not names are familiar (91% correct for M.S., 92% for P.H.); for faces, however, M.S. and P.H. both perform at chance level (52% correct for M.S., 51% for P.H.).
VISUAL KECOGNITION
181
Table 1. Numbers of familiar faces and familiar names correctly selected by MS., P.H. and by normal subjects in a forced-choice task (data for P.H. and normal subjects from YOUNG and DE HAAN 1221)
MS
PH Norma1 Subjects
Faces
Names
6-i
116
65 125.50 3.33
118 127.50 0.84
In summary, then. M.S. shows a marked object agnosia and complete prosopagnosia on clinical tests, but remains able to read. RATCLIFF and NEW-COMBE[15] suggested that his impairment atfects the construction of object-centred visual representations.
INVESTIGATION
OF COVERT
RECOGNITION
The possibility of covert recognition was investigated for MS. using four tasks. Two tasks (semantic priming of name recognition, and learning face-name pairings) were taken from those used to demonstrate covert recognition of familiar faces by PH. [S, 241. The other two tasks (semantic priming of object recognition, and object matching) were intended to investigate whether there was any covert object recognition.
FACE Task 1: Semantic
priming
RECOGNITION
of name recognition
In this task M.S. was asked to classify printed target names as belonging to familiar (famous) or unfamiliar (not famous) people. Each name was immediately preceded by a face prime or by a name prime presented for 500 msec. We sought to determine whether or not the presence of a related prime facilitated classification of the target name. YOUNG et al. [24] found that P.H. showed equivalent facilitation from face primes (which he was very poor at recognizing overtly) and from name primes (which he could easily identify). Stimuli and procedure. Stimuli were the same as those used by YOU&G et al. 124, Experiment 4J with P.H. targets consisting of printed names of 10 pairs of associated famous people (e.g. Prince Charles and Prmcess Diana) and 20 unfamiliar people. Targets were presented one at a time on back-projected slides, and were preceded by face primes or by name primes in separate blocks of trials. Face and name stimuli subtended horizontal visual angles of approx. 6”. For familiar target names the primes were faces or names of Related (e.g. Princess Diana’s face before Prince Charles’s name), Neutral (an unfamiliar face before Prince Charles’s name), or Unrelated (Ronald Reagan’s face before Prince Charles’s name) people. For unfamiliar target names two-thirds of the primes were faces or names of the familiar people, and one-third of primes consisted of an unfamiliar face or an unfamiliar name, so that the primes themselves had no cue value in predicting whether or not a familiar target name would follow. Primes were presented for 500 msec, and targets for 4 sec. M.S. was asked to decide whether or not each target name was that of a famous person, and manual reaction times to the target names (made by moving a vertical lever toward his body for famous target names and away from his body for nonfamous target names) were recorded from target stimulus onset. He was informed that each target would be preceded by a briefly presented stimulus, and asked to look at this stimulus but make no response to it. Four blocks of 120 trials were run in separate sessions spread across 2 days, involving name primes, face primes, face primes, and name primes in that order. Within each block of trials each of the 20 familiar names was used once as a target in Related, Neutral and Unrelated priming conditions, with the remaining 60 trials involving the unfamiliar target names. Order of presentation of familiar and unfamiliar target names, and Related, Neutral, or Unrelated primes, was unpredictable. On some of the practice trials placed at the beginning of each testing session we asked MS. to report both the
182
FREDANEWCOMBE,ANDREW W. YOUNG and EDWARD H. F. DE HAAN
prime and the target by naming them aloud. He was easily able to report name primes despite the brief (500 msec) presentation used, but could not report face primes. At the end of the final sessions of the task MS. was shown all of the faces used (with unlimited exposure), told that these belonged to the familiar people whose names he had been classifying. and asked to identify them. He was unable to identify any correctly.
Results. MS. made few errors (overall error rate ~2%). Mean reaction times for his correct responses to target names of unfamiliar (nonfamous) and familiar (famous) people preceded by Related, Neutral, or Unrelated face or name primes are given in Table 2. Table 2. Mean reaction times (in msec) for M.S.‘s correct responses to target names of familiar and unfamiliar people preceded by Related, Neutral, or Unrelated face or name primes (Task 1) Familiar
Face primes Name primes
targets
Related prime
Neutral prime
1260 I178
1276 1370
Unrelated prime 1264 1439
Unfamiliar targets 1810 1872
Mean correct reaction times for each familiar target name in each condition were calculated, and submitted to a two-factor analysis of variance to determine the effects of prime Domain (faces or names; repeated measure) and prime Type (Related, Neutral, or Unrelated; repeated measure). This method of analysis is the same as that used by YCKJNGet al. [24, Experiment 41 with P.r1. For M.S., the effect of prime Domain did not reach statistical significance [P (1, 19) = 3.35,0.1> P> 0.051, but there was a significant effect of prime Type [F (2,38) = 5.48, P-c 0.011. The most important finding, however, was the prime Domain x prime Type interaction [F (2, 38)=6.38, P
VISUAL
183
RECOGNITION
present even to our own faces, which he had only encountered since his accident [S; Task 73. Hence it is evident that for P.H., covert recognition can be found even to faces that have never been recognized overtly. Clearly this is not the case for M.S. In order to determine whether covert recognition might, however, be found for people who were famous before M.S.‘s illness we used a face-name learning task. Tusk 2: Leurniny face-name
pairings
In this task M.S. was asked to learn true (face + correct name) or untrue (face + another person’s name) pairings of names and faces. DE HAAN et al. [S] showed that in such tasks the prosopagnosic patient P.H. was better at learning true than untrue pairings. In order to investigate the possibility of covert recognition of faces of people who were famous before M.S. became ill the task was run twice, once using faces of people famous in the 1960’s and once using more recently famous faces. Stimuli und procedure. MS. was shown a series of photographs of faces of famous people, and given two alternative names for each. These names were the correct (true) name and a different name belonging to a person of comparable age from the same occupational category. For example, he was asked whether Paul McCartney’s face was that of Paul McCartney or Mick Jagger. The faces used in the learning task were selected from those to which he answered incorrectly on this screening task. Thus they were faces for which MS. had failed to show overt recognition in a binary discrimination; this criterion for absence of overt recognition is the same as that used in our work with P.H. [g, Task 71. Six faces of people famous in the 1960’s that met this criterion were spread out before MS. in a random 3 x 2 matrix, and he was twice instructed as to which name went with each face. Three faces were paired with true (correct) names; these were those of Tony Benn, Bobby Charlton and Ernie Wise. The other three faces (John Kennedy, Paul McCartney, Elvis Presley) were paired with untrue (exchanged) names (John Kennedy named as “Elvis Presley”, Elvis Presley identified as “Paul McCartney”, and Paul McCartney called “John Kennedy”). The test contained I2 trials, begun by rearranging the faces in the 3 x 2 matrix into a new order. M.S. was then asked to point to the paacecorresponding to a name that was given orally. If he made a mistake he was corrected. All six names were tested in a different order on each trial. Two days later, an equivalent test was given using six faces of people who have become famous since 1970. Faces of Jimmy Carter, Jack Nicholson and Norman Tebbit were paired with true (their own) names, and untrue (exchanged) pairings were created for the faces of Paul Daniels, Norman Fowler and Michael Parkinson.
Results. The number of times M.S. pointed to the correct face was separately determined for true pairings and for untrue pairings for each trial (max = 3 correct for any trial). Raw scores for 1960’s and post-1970 faces are shown in Table 3. Our method of analysing these data was the same as that used by DE HAAN et ul. [S] for similar learning tasks carried out with P.H. The sign test was used to compare performance with true and untrue pairings by scoring each trial as “+” (better on true than untrue pairings) “=” (equal performance with true and untrue pairings), or “ -” (better performance with untrue than true pairings). No difference was found either for 1960sfaces (3+ ,4=, S-, P>O.l) or for post-1970faces (5 +, 4=, 3-, P>O.l). Table 3. Numbers
of correct
choices
(max = 3) of face to match stated names on each trial of the face-name learning task (Task 2)
I 1960s faces Post-1970
faces
2
3
True pairings Untrue pairings
100020221213 002223123121
True pairings Untrue pairings
210312003222 2 110
4
5
11
Trial 6 I
8
9
2
2
11
10
11
12
2
1
184
FREDA NEWCOMBE. ANDREW W. YOUNG and EDWARD H. F. DE HAAN
Discussion. The results of this task provide no evidence ofcovert recognition for MS, either for faces of people famous before (1960s) or since (post-1970) his illness. Tasks 1 and 2 were thus consistent in finding that MS does not show covert recognition of familiar faces. In Tasks 3 and 4 we investigated whether he would show covert recognition of visually-presented objects.
OBJECT Tusk 3: Semantic
priming
RECOGNITION
of word recognition
The rationale for this task is similar to that of Task 1. MS. was asked to classify printed targetstimuliasbeingfamiliarwordsorpronounceablenonwords(lexicaldecision task).Each target was immediately preceded by a prime consisting of a photograph of an object presented for 500 msec. We were interested in determining whether or not the presence of a related object facilitated lexical decisions to target words. Facilitation of word recognition following presentation of related object primes is known to occur for normal subjects [19,21]. Stimuli and procedure. Two sets of 20 picture primes (photographs of objects) and word targets were created, such that each picture was of an object that was closely related to the word’s referent (e.g. a picture of a ring and the word “finger”, a picture of a nail and the word “hammer”). The words in these sets of related prime-target pairs were roughly matched for frequency. A list of the primes and targets from each set is given in Appendix 1. One set of prime-target pairs was then scrambled, so that the picture primes and word targets were Unrelated to each other, the other set was left to form the Related condition of the experiment. On each trial MS. was shown a back-projected picture prime for 500 msec, followed by a target word or a pronounceable nonword for 4 sec. Nonwords were created by changing one or two letters of nouns not used in the experiment. He was asked to decide as quickly and accurately as possible whether the target was a word or a nonword, and his reaction times (timed from target stimulus onset) were recorded from switches mounted in the vertical lever used to make his responses (with lever movement toward his body used to signal “word” responses, movement awayfrom his body for “nonword’responses). As for Experiment 1, MS. was told that each target would be preceded by a briefly presented stimulus, and was asked to look at this stimulus but make no response to it. The picture primes subtended visual angles of approx 6”. Eighty trials were run, involving the 20 Related picture-word pairs, the 20 Unrelated (scrambled) pairs, and 40 trials with a picture of a familiar object followed by a nonword target. These trials were arranged into an unpredictable order. At the end of the session MS. was shown all of the picture primes one at a time (with unlimited exposure), and asked to name them as quickly as possible. His response times were recorded using a voice key. The task was repeated a day later, but with the sets of stimuli used to create Related and Unrelated pairs reversed (i.e. the Related pairs from day 1became the Unrelated pairs for day 2). Six months later this entire procedure (both sessions) was repeated. The essential features of this design, then, are that MS. carried out a lexical decision task to target stimuli preceded by picture primes presented for 500 msec. These pictures were of objects that could be Related or Unrelated to target words.
Results. At the end of each of the four sessions, M.S. was tested for his ability to identify the primes used. He was able to identify a number of them, though his mean reaction time for those he could identify (i.e. name) correctly was 5095 msec. Table 4 summarizes his ability to identify the primes across these four sessions. For each prime we have calculated whether it was recognized on all four occasions, on three occasions, two occasions, one occasion, or not at all. Raw data are included in Appendix 1. Table 4 shows how the 40 primes used were distributed across these categories. It is clear that most primes were consistently recognized or consistently not recognized. A few primes (4) were, however, equally often recognized or not recognized; these were eliminated from consideration. The remaining primes were divided into 15 that were usually recognized (i.e. recognized on 3 or 4 occasions) and 21 that were usually not recognized (recognized on 0 or 1 occasions). Each of these primes had been used twice with a Related word and twice with an Unrelated
VISUAL
Table 4. Number
Number
RECOGNITION
of primes recognized
of primes
185
in 4, 3, 2, 1, or 0 of the four post-tests
4
Number 3
11
4
of times recognized 2 1 4
0
2
19
word across the four sessions. Thus mean reaction times could be calculated for correct responses to target words preceded by recognized or unrecognized primes in Related and Unrelated conditions. Mean reaction times for correct responses to word targets preceded by recognized or unrecognized primes are shown in Table 5. M.S. made few errors in the lexical decision task (overall error rate < 2%). His mean reaction time for “nonword” responses was 1890 msec.
Table 5. Mean reaction times (in msec) for correct responses to target words preceded by Related or Unrelated picture primes that M.S. could or could not identify in the post-test
Prime recognized (A’= 15) Prime not recognized (N=21)
Related
Unrelated
1329 1600
1717 1.585
An unequal cells analysis of variance of the correct reaction times to word targets was carried out to determine the effects of prime Type (Related or Unrelated; repeated measure) and prime Recognition (prime usually recognized or not usually recognized in the post-test). There was no overall difference in reaction times to target words preceded by recognized or unrecognized primes (F-C l), and the main effect of prime Type did not reach statistical significance [F (1, 34)=3.15, O.l> P>O.O5]. There was, however, a significant prime Type x prime Recognition interaction [F (1, 34) = 5.31, PC O.OS], Tukey tests (X = 0.05) showed that responses for words preceded by Related primes that M.S. could recognize in the post-test were faster than responses in the other three cells of the analysis, which did not differ from each other. Discussion. The analysis of potential covert effects in object recognition tasks is complicated by the fact that M.S. is able to identify a substantial proportion of presented objects. Once the picture primes are separated into those he can and cannot usually recognize, however, it is clear that semantic priming was only obtained for primes that M.S. could overtly identify. Hence, as for faces, there is no evidence of covert recognition of objects he cannot identify. It is interesting, though, that M.S.‘s reaction times for overt identification should be so long (5095 msec) when the priming effect can be shown to a 500 msec presentation. We suspect that part of the reason for his long reaction times for overt identification reflects caution created by loss of confidence in his own visual recognition abilities. Because of constraints on the number of photographs of objects available to us when Task 3 was constructed, a Neutral prime condition was not included. Since there was no evidence of priming from unrecognized objects, however, these might themselves be considered to form a Neutral condition. The fact that reaction times for target words
186
FKEDA NEWCOMLIE,ANDKEW W. YOUNG and EDV~AKDH. F. DE HAAPG
preceded by Related primes that M.S. could recognize were faster than reaction times in the remaining three word target conditions (which did not differ from each other) would then indicate that the semantic priming effect from pictures he can recognize is one of facilitation without inhibition. The results of Task 3, then, imply that M.S. does not show covert recognition of objects he is unable to identify overtly. In order to confirm this conclusion by a different method, Task 4 employed an object matching task. Task 4: Object matching
M.S. is able to match photographs to determine whether they show same or different objects, provided that the difference in views is not too extreme. We thus decided to investigate whether or not he would be able to match views of unrecognized familiar objects more quickly than he could match views of unfamiliar objects. The logic of this procedure is the same as that used for face matching tasks by DE HAAN et al. [S, Tasks 1 and 21; covert recognition would produce faster matching of unrecognized familiar objects than unfamiliar objects. Stimuli and procedure. Two photographs were taken of each of 53 familiar everyday objects and 53 unfamiliar objects. The 53 unfamiliar objects represented as many as we could find after a fairly diligent search; they included pieces of hospital and laboratory equipment, machine fittings. obscure car spares, parts of broken household utensils, unusual electrical fittings, and so on. All of these unfamiliar objects achieved a very low mean familiarity in a set of ratings made by six normal people of M.S.‘s age. Photographs were taken from a range of angles, with no attempt to standardize these: we relied instead on the sheer number of pairs to control for differences in camera angle. Slides ofthese object photographs were presented (back-projected) to MS. in pairs, with one positioned vertically above the other. Examples of “same” pairs of famihar and unfamiliar objects are shown in Fig. I. Each of the 53 familiar pairs and 53 unfamiliar pairs was presented once in the course of the experiment, and each of these photographs was also used once as a member of a pair of photographs of different objects. Each pair of photographs was presented for 4 set, and MS. was asked to decide whether or not they showed same or different objects. Responses (timed from stimulus onset) were made using the lever mechanism already described (with movement toward his body used to signal “same”, and away from his body to signal “different”). “Same” and “different” pairs, and pairs involving familiar or unfamiliar objects, were arranged into random order. The experiment was divided into two separate sessions, with a 6-month interval in between. At the end of each session MS. was shown all the stimuli that had been used in that session with unlimited presentation time. and asked to identify (i.e. name) the objects in the “same” pairs.
Results. Only reaction times to “‘same” pairs were analysed. It is possible to separate reaction times to the “same” pairs into those to objects which M.S. could or could not recognize in the test of overt recognition given at the end of each experimental session. This cannot be done for responses to “different” pairs where M.S. may recognize either, both or neither of the objects. His mean reaction times for correct responses to different pairs were 2075 msec for familiar pairs and 2186 msec for unfamiliar pairs, with 52/53 responses correct to each type of pair. Reaction times to “same” pairs were separated for analysis into those to familiar objects that were or were not recognized in the post-test, and those to unfamiliar objects. Mean correct reaction times are presented in Table 6. The MannWhitney U-test was used to compare reaction times to recognized and not recognized familiar pairs, showing that the objects which could be recognized on the post-test were matched more quickly (nI =23, n2 =28, lJ=430.5, ~=2.05, 2-tailed P~0.05). There was, however, no difference between reaction times for familiar pairs which could not be recognized and unfamiliar pairs (trl = 28, n,=49, U=812, z= 1.33, 2-tailed P>O.l).
VISUAL
RECOGNITION
FAMILIAR FIG. 1. Examples
187
UNFAMILIAR of “same” pairs of familiar
and unfamiliar
objects (Task 4).
VISUAL
RECOGNITION
189
Table 6. Mean correct reaction times (in msec) for correct matching of “same” pairs of familiar objects that were or were not recognized in the post test, and “same” pairs of unfamiliar objects (Task 4) Familiar
objects
Recognized
Not recognized
Unfamiliar objects
1886 N=23
2401 N=28
2529 N=49
Discussion. As for Task 3, there is no evidence of covert recognition. Instead, it is clear that MS. is only better able to match views of familiar objects that he can recognize overtly. GENERAL
DISCUSSION
Our findings point consistently to the same conclusion; MS. does not show covert recognition. In Task 1 semantic priming of name recognition was obtained from name primes but not from face primes. In Task 2 M.S. showed no advantage for learning true rather than untrue face-name pairings, both for faces of people famous before his illness and for faces of people who have become famous since he was ill. In Task 3 semantic priming of lexical decision was obtained only from picture primes that MS. was able to recognize overtly. In Task 4 faster matching of “same” pairs of photographs of familiar than unfamiliar objects was again found only for objects that M.S. could recognize overtly. For MS.. then, his ability to recognize faces and objects is much the same whether it is tested with tasks demanding implicit or explicit recognition. M.S.‘s performance is thus different to that of the patient P.H. [S], w”lo showed evidence of ability to recognize familiar faces on implicit but not on explicit tasks. This finding of a difference between M.S. and P.H. is particularly interesting because on tests of overt face recognition ability there is no apparent difference between P.H. and M.S. (see Table 1); both are unable to recognize familiar faces overtly. But the pattern of covert recognition effects shown by P.H. on implicit tests is not found for MS. It seems unlikely that the difference in elapsed time since injury might be important in accounting for the presence or absence of covert recognition in M.S. and P.H. We investigated P.H.‘s covert recognition abilities some 5 to 6 yr after his accident, whereas the present work with MS. has been conducted some 16 to 17 yr after his illness. One could perhaps speculate that covert recognition effects might simply die away once overt recognition is no longer possible. However, the 5-6 yr interval between P.H.‘s injury and our testing sessions is itself considerable, yet we were able to demonstrate that P.H. showed covert recognition even to faces of people he had only met since his accident [S]. Thus for P.H. there is no sign of covert recognition tailing off, and it is found even for faces he has never been able to recognize overtly. The difference between M.S. and P.H. that we consider crucial is that M.S. shows more obvious signs of higher-order perceptual impairment. He has a marked object agnosia, and performs very poorly on face matching tasks. P.H. is himself not completely free from problems in object recognition and face matching tasks, but his difficulties do not approach the severity of those experienced by M.S.; M.S. is clearly agnosic in daily life, whereas P.H.‘s problems with object recognition show up only in formal tests. The existence of higher-order
190
FREDA NEWCOMBE.ANDREWW. YOUNG and EDWARDH. F. DE HAAN
perceptual impairment for M.S. means that he is probably unable to construct visual representations adequate for the recognition of faces and many everyday objects. In BRUCE and YOUNG’S [S] terms MS’s impairment affects structural encoding. Without adequate structural encoding neither overt nor covert recognition will be possible. This conclusion is consistent with BAUER’S[3] failure to find evidence ofcovert recognition offamiliar faces in the skin conductance responses of the patient G.Y ., who had a marked apperceptive impairment. The differences between MS. and P.H., then, are consistent with the distinction between perceptual and mnestic forms of prosopagnosia emphasized by DE RENZI [9]. It is thus possible that presence or absence of covert recognition of familiar faces will provide an additional index of these contrasting types of face recognition impairment.
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IY. 20. 21, 22. 23. 24.
und
of the guilty knowledge test. Neuropsychologia 22,457469, 1984. BAUER, R. M. The cognitive psychophysiology of prosopagnosia. In Aspects of Face Processing, H. D. ELLIS,M. A. JEEVES,F. NEWCOMLIEand A. YOUNG (Editors), pp. 253%267. Martinus Nijhoff, Dordrecht, 1986. BOUAMER,J. Die Prosop-Agnosie. Archiv Jk Psychiatric und Nervenkrankheiten 179, 6&53, 1947. BRUCE, V. and YOUNG, A. W. Understanding face recognition. Br. J. Psychol. 77, 305-327, 1986. DAMASIO, A. R., DAMASIO, H. and VAN HOESEN, G. W. Prosopagnosia: anatomic basis and behavioral mechanisms. Neurology 32, 331-341, 1982. DE HAAN, E. H. F., YOUNG, A. and NEWCOMBE,F. Faces interfere with name classification in a prosopagnosic patient. Cortex 23, 309 316, 1987a. DE HAAN, E. H. F., YOUNG, A. and NEWCOMBE,F. Face recognition without awareness. Cognir. Neuropsychol. 4, 385-415, 1987b. DE RENZI, E. Current issues in prosopagnosia. In Aspects of face Processing, H. D. ELLIS, M. A. JEEVES, F. NEWCOMBEand A. YOUXG (Editors), pp. 243- 252. Martinus Nijhoff, Dordrecht, 1986. H~(.AEN, H. The neuropsychology of face recognition. In Perceiving and Remembering Fuces, Cr. DAVIES, H. ELLIS and J. SHEPHERD (Editors). pp. 39-53. Academic Press, New York, 1981. H&AEN, H. and ANGELERGLXS,R. Agnosia for faces (prosopagnosia). Arch.? Neural. 7, 92- 100. 1962. MEADOWS, J. C. The anatomical basis of prosopagnosia. J. Naurol. Nettrosurg. Psychiut. 37, 489-501, 1974. NEWCOMBE,F. and RATCLIFF, G. Agnosia: a disorder of object recognition. In Les Syndromes de Disconnexion Culleuse chez /‘Hornme, F. M~CHEL and B. SCHOTT (Editors), pp. 317--341. Colloque International de Lyon, Lyon, 1975. POSNFR, M. I. and SNYL)EK,C. R. R. Facililation and inhibition in the processing of signals. In Artrntion and Pwformance. P. M. A. RABBITT and S. DORNIC (Editors), pp. 669-682. Academic Press, London, 1975. RAYTLIFFE,G. and NEWTOMBE,F. Object recognition: some deductions from the clinical evidence. In Normalit) and Pathology in Cognitive Functions. A. W. ELLIS (Editor). pp. 147- 171. Academic Press, London, 1982. SAE~RAN, E. M. and MAWIN. 0. S. M. Reading without phonology: evidence from aphasia. Q. /. e.up. Psycho/. 29, 515 -525, 1977. SctlACTER, D. L. Implicit memory: history and current status. J. esp. Psychol.: Lrurn. k/em. (‘ognil. 13, 501 518, 1987. SCHACTFR, D. L., MCANDREWS, M. P. and Mos~(>vIT(.H. M. Access to consciousness: dissociations between implicit and explicit knowledge in neuropsychological syndromes. In Thouqhl Withour Lunyuaye, I.. WEISKKANTZ (Editor). Oxford University Press, Oxford, 1988. SPERRER, R. D., MTCAULEY, C., RAGAIN. R. D. and WFIL, C. M. Seman!ic priming effects on picture and word processing. Mem. Coynil. 7, 339-345, 1979. TRANEL, D. and DAMASIO, A. R. Knowledge without awareness: an autonomic index of facial recognition by prosopagnosics. Science 228, 1453-1454, 1985. VAtJDERwART. M. Priming by pictures in lexical decision. J. oerh. Learn. verb. Behap. 23, h7- 83, 1984. YOUNG, A. W. and DE HAAN, E. H. F. Boundaries of covert recognition in prosopagnosia. Cognil. Neuropsychol. 5, 317-336, 1988. YOUNG, A. W., HAY, D. C.. MCWEENY, K. H., FLUDE, 8. M. and ELLIS, A. W. Matching familiar and unfamiliar faces on internal and external features. Perception 14, 737-746. 1985. YOUNG, A. W., H~LLAWLLL, D. and DE HAAN, E. Cross-domain semantic priming in normal subjects and a prosopagnosic patient. Q. J. ewp. Psycho/. 40A, 1988.
VISUAL
RECOGNITION
APPENDIX
191
1
List of picture primes and word targets used in Task 3. Numbers in brackets indicate the number (max = 4) MS. was able to identify each prime overtly in the four post-test sessions Set
1
Picture Pushchair Bread Vacuum cleaner Clothes peg Paint Mirror Shoes Camera Matches Lawnmower Shears Watch Rake Crash helmet Safety pin Violin Boat Aeroplane Envelope Tennis ball
Set 2 Word
(2) (0) (0) (0) (0) (2) (4) (3) (0) (0) (1) (4) (0) (0) (0) (0) (0) (4) (4) (0)
Butter Carpet Clothes Door Face Feet Film Fire Grass Hedge Hour Leaves Motorcycle Nappy Orchestra Sea Sky Stamp Tennis
Word
Picture Trumpet Head Biscuits Pie Kettle Glasses Ring Comb Lipstick Hammer Pencil Scissors Bed Car Frying pan Iron IJmbrella Bucket Track shoes Grapes
;:I (3) (0) (2) (4) (2) (4) 1:; (4) (4) (0) (3) (0) (0) (4) (1) (4) (0)
Band Body Cheese Chips Coffee Eyes Finger Hair Mouth Nail Paper Paste Pyjamas Road Sausages Shirt Shower Spade Sport Wine
of times
PROSOPAGNOSIA
1989.
0028-3932.89 53.00+000 c’ 1989 Pergamon Press plc
AND OBJECT AGNOSIA RECOGNITION*
WITHOUT
COVERT
FREDANEWCOMBE,?ANDREW W. YOUNG and EDWARD H. F. DE HAANt tMRC
Neuropsychology Unit, Radcliffe Infirmary, Woodstock Road, Oxford OX2 6HE, U.K.; and Psychology Department, Lancaster University, Bailrigg, Lancaster LA1 4YF, U.K. Receiced
14 March 1988; accepted
11July 1988)
Abstract-Investigations of the visual recognition abilities of the patient M.S. are reported. MS. is unable to achieve overt recognition of any familiar faces, and many everyday objects. In Task 1 he showed semantic priming from name primes but not from face primes in a name recognition task. In Task 2 he showed no advantage in learning true (face+correct name) rather than untrue (face+someone else’s name) pairings of faces and names. In Task 3 semantic priming of lexical decision was only found for object picture primes that M.S. was able to recognize overtly. In Task 4 faster matching of photographs of familiar than unfamiliar objects was only found for objects that MS. was able to recognize overtly. These findings demonstrate an absence of covert recognition effects for MS., consistent with the view that his impairment is primarily “perceptual” in nature.
INTRODUCTION
PROSOPAGNOSK patients are no longer able to recognize familiar people from their faces. The deficit can extend to even the most well-known faces including friends, family, famous people and the patient’s own face when seen in a mirror [4, 6, 10, 111. Recent studies have, however, shown that despite the almost complete breakdown of overt face recognition ability found in some cases of prosopagnosia, covert recognition may continue to take place. This covert recognition can be demonstrated in certain tasks which test recognition implicitly. BAUER [2, 31 and TRANEL and DAMASIO [ZO], for instance, demonstrated covert recognition in the form of autonomic responses to familiar faces. Similarly, DE HAAN et al. [7, S] demonstrated covert recognition using behavioural measures derived from performance in matching, learning, and interference tasks, and YOUNG et a[. [24] found semantic priming from unrecognized faces onto the recognition of name targets (for example, from seeing Princess Diana’s face to recognizing Prince Charles’s name as familiar). The existence of covert recognition allows prosopagnosia to be considered as one of a group of neuropsychological impairments characterized by what SCHACTER et al. [l S] term failures of access to consciousness. The patient’s face recognition abilities are in a sense quite well preserved, but he or she does not realize this because face recognition takes place without the normal awareness of recognition. A central issue concerns whether covert recognition is to be found for all prosopagnosic patients, or whether it only exists for a particular type of face recognition impairment. One reason for expecting the latter is that neuropsychologists interested in prosopagnosia have * This research was supported by MRC grant PC 7301443 to Freda Newcombe grant G 8519533 to Andy Young. We are grateful to the Press Association photographs of faces to use as stimuli. 179
and John Marshall, and by MRC for help in obtaining suitable
180
FREUA NEWCOMB~, ANDREW W. YOUNGand EDWARD
H. F. DE HAAN
often made a distinction between two forms of the disorder [9, 10, 121. In one form the underlying cause seems to be impairment of the highest levels of visual perception; the patients are poor at matching views of unfamiliar faces and there is usually an associated visual object agnosia [9]. In the other form of prosopagnosia ability to match views of unfamiliar faces and to recognize everyday objects is relatively intact, and the problem seems to take the form of a material-specific memory impairment (in the sense that memories concerning familiar people cannot be accessed from an adequately perceived face, yet remain accessible from other inputs, such as names or voices). Given the hypothesized existence of these perceptual and mnestic forms of prosopagnosia it is tempting to speculate that covert recognition is linked to the form involving the materialspecific memory impairment. This view would be consistent with the parallel that can be drawn between covert recognition of familiar faces in prosopagnosia and the priming and implicit memory phenomena found in cases of amnesia [17, 181. The corollary of this view is that covert recognition may not exist for the form of prosopagnosia involving the primarily perceptual impairment, an hypothesis first suggested by BAUER [3]. The present paper investigates this possibility with the patient MS., previously studied by NEWCOMBE and RATCLIFF [13] and RATCLIFF and NEWCOMBE [IS], and thought to have a higher-order perceptual impairment.
CASE DESCRIPTION MS. is a former police cadet who contracted a febrile illness in 1970, at the age of 23. The presumptive diagnosis was herpes encephalitis, but this was never confirmed by viral antibody studies. A full case description has been given by NEWCOMBEand RATCLIFF [I 31 and RAT~LIFF and NEWCOMHE[ 151, so we will only summarize the essential features of previous reports and add some new details. M.S. has a left homonymous hemianopia, but his visual acuity is normal (6/6; N5 for near vision). His colour vision is, however, severely impaired. He also has a severe object agnosia which affects his ability to recognize both real objects and object pictures. MS. can often identify a real object more readily than a picture of the same object. but his performance with both types of stimuli is ciearly defective. He was able to successfully identify only 8/36 line drawings, whereas he could name 20/36 of the same objects from verbal descriptions of their functions. He can, though, make accurate copies of drawings he has not recognized, using a line-by-line copying strategy. The fact that M .S. could only identify 20/36 objects from verbal descriptions of their functions shows that there is some impairment of semantic memory, and this IS particularly evident in tasks involving living things. Despite this, MS. remains able to read, and his performance at making “true or false”judgements about absurd sentences (46/50) is within normal limits. His readingofsingle words is accurate (94/3CO correct for regular and exception words from BAUER and STANOVICH[l]) and he can also make accurate lexical decisions (one error to the list from SAFFKANand MARIN 1161). M.S. is completely unable to recognize familiar faces. On a test involving the faces of 20 highly familiar, ?O moderately familiar, and 20 unfamiliar people he could identify no one. He was also poor at matching photographs of unfamiliar people. His score was 33/54 on the Benton Test of facial recognition (5/‘6 correct responses when matching identical views, 13/24 with changed orientation, and 15124 with changed lighting), and he only managed 49/80 correct trials in our own task of matching internal or external facial features 123; Experjment I]. This is usually given as a reaction time task, but M.S.‘s low level of performance made meaningful measurement of reaction times impractical. The mean accuracy of normal subjects when performing this task was 74.4180 correct (SD = 3.X3). MS. was also poor at matching facial expressions (25,!32 correct; normal subjects U= 29.82. SD =0.37), and relied on a strategy of comparing first the eyes rnd then the mouth (which suggests that he could not take in the appearance of the face “as a whole”). A forced-choice task was used to compare M.S.‘s ability to recognize faces and names. This task has been described in detail by YOUNGand DE HAAN1221, and consists of 128 pairs of faces and 128 pairs of names. One stimulus in each pair is a familiar person’s face or name, and one is an unfamiliar person’s face or name. The membcra of each pair of faces or names were simultaneously presented, one above the other. M.S. was asked to choose the fami!iar’member of each pair. His performance is-cbmpared with that of the prosopagnoslc patient P.H. 1221 in Table 1. MS’s performance is very similar to that of P.H. Although MS. and P.H. are both impaired for forcedchoice name familiarity decision in comparison with normal subjects, they are none-the-less highly accurate at determining whether or not names are familiar (91% correct for M.S., 92% for P.H.); for faces, however, M.S. and P.H. both perform at chance level (52% correct for M.S., 51% for P.H.).
VISUAL KECOGNITION
181
Table 1. Numbers of familiar faces and familiar names correctly selected by MS., P.H. and by normal subjects in a forced-choice task (data for P.H. and normal subjects from YOUNG and DE HAAN 1221)
MS
PH Norma1 Subjects
Faces
Names
6-i
116
65 125.50 3.33
118 127.50 0.84
In summary, then. M.S. shows a marked object agnosia and complete prosopagnosia on clinical tests, but remains able to read. RATCLIFF and NEW-COMBE[15] suggested that his impairment atfects the construction of object-centred visual representations.
INVESTIGATION
OF COVERT
RECOGNITION
The possibility of covert recognition was investigated for MS. using four tasks. Two tasks (semantic priming of name recognition, and learning face-name pairings) were taken from those used to demonstrate covert recognition of familiar faces by PH. [S, 241. The other two tasks (semantic priming of object recognition, and object matching) were intended to investigate whether there was any covert object recognition.
FACE Task 1: Semantic
priming
RECOGNITION
of name recognition
In this task M.S. was asked to classify printed target names as belonging to familiar (famous) or unfamiliar (not famous) people. Each name was immediately preceded by a face prime or by a name prime presented for 500 msec. We sought to determine whether or not the presence of a related prime facilitated classification of the target name. YOUNG et al. [24] found that P.H. showed equivalent facilitation from face primes (which he was very poor at recognizing overtly) and from name primes (which he could easily identify). Stimuli and procedure. Stimuli were the same as those used by YOU&G et al. 124, Experiment 4J with P.H. targets consisting of printed names of 10 pairs of associated famous people (e.g. Prince Charles and Prmcess Diana) and 20 unfamiliar people. Targets were presented one at a time on back-projected slides, and were preceded by face primes or by name primes in separate blocks of trials. Face and name stimuli subtended horizontal visual angles of approx. 6”. For familiar target names the primes were faces or names of Related (e.g. Princess Diana’s face before Prince Charles’s name), Neutral (an unfamiliar face before Prince Charles’s name), or Unrelated (Ronald Reagan’s face before Prince Charles’s name) people. For unfamiliar target names two-thirds of the primes were faces or names of the familiar people, and one-third of primes consisted of an unfamiliar face or an unfamiliar name, so that the primes themselves had no cue value in predicting whether or not a familiar target name would follow. Primes were presented for 500 msec, and targets for 4 sec. M.S. was asked to decide whether or not each target name was that of a famous person, and manual reaction times to the target names (made by moving a vertical lever toward his body for famous target names and away from his body for nonfamous target names) were recorded from target stimulus onset. He was informed that each target would be preceded by a briefly presented stimulus, and asked to look at this stimulus but make no response to it. Four blocks of 120 trials were run in separate sessions spread across 2 days, involving name primes, face primes, face primes, and name primes in that order. Within each block of trials each of the 20 familiar names was used once as a target in Related, Neutral and Unrelated priming conditions, with the remaining 60 trials involving the unfamiliar target names. Order of presentation of familiar and unfamiliar target names, and Related, Neutral, or Unrelated primes, was unpredictable. On some of the practice trials placed at the beginning of each testing session we asked MS. to report both the
182
FREDANEWCOMBE,ANDREW W. YOUNG and EDWARD H. F. DE HAAN
prime and the target by naming them aloud. He was easily able to report name primes despite the brief (500 msec) presentation used, but could not report face primes. At the end of the final sessions of the task MS. was shown all of the faces used (with unlimited exposure), told that these belonged to the familiar people whose names he had been classifying. and asked to identify them. He was unable to identify any correctly.
Results. MS. made few errors (overall error rate ~2%). Mean reaction times for his correct responses to target names of unfamiliar (nonfamous) and familiar (famous) people preceded by Related, Neutral, or Unrelated face or name primes are given in Table 2. Table 2. Mean reaction times (in msec) for M.S.‘s correct responses to target names of familiar and unfamiliar people preceded by Related, Neutral, or Unrelated face or name primes (Task 1) Familiar
Face primes Name primes
targets
Related prime
Neutral prime
1260 I178
1276 1370
Unrelated prime 1264 1439
Unfamiliar targets 1810 1872
Mean correct reaction times for each familiar target name in each condition were calculated, and submitted to a two-factor analysis of variance to determine the effects of prime Domain (faces or names; repeated measure) and prime Type (Related, Neutral, or Unrelated; repeated measure). This method of analysis is the same as that used by YCKJNGet al. [24, Experiment 41 with P.r1. For M.S., the effect of prime Domain did not reach statistical significance [P (1, 19) = 3.35,0.1> P> 0.051, but there was a significant effect of prime Type [F (2,38) = 5.48, P-c 0.011. The most important finding, however, was the prime Domain x prime Type interaction [F (2, 38)=6.38, P
VISUAL
183
RECOGNITION
present even to our own faces, which he had only encountered since his accident [S; Task 73. Hence it is evident that for P.H., covert recognition can be found even to faces that have never been recognized overtly. Clearly this is not the case for M.S. In order to determine whether covert recognition might, however, be found for people who were famous before M.S.‘s illness we used a face-name learning task. Tusk 2: Leurniny face-name
pairings
In this task M.S. was asked to learn true (face + correct name) or untrue (face + another person’s name) pairings of names and faces. DE HAAN et al. [S] showed that in such tasks the prosopagnosic patient P.H. was better at learning true than untrue pairings. In order to investigate the possibility of covert recognition of faces of people who were famous before M.S. became ill the task was run twice, once using faces of people famous in the 1960’s and once using more recently famous faces. Stimuli und procedure. MS. was shown a series of photographs of faces of famous people, and given two alternative names for each. These names were the correct (true) name and a different name belonging to a person of comparable age from the same occupational category. For example, he was asked whether Paul McCartney’s face was that of Paul McCartney or Mick Jagger. The faces used in the learning task were selected from those to which he answered incorrectly on this screening task. Thus they were faces for which MS. had failed to show overt recognition in a binary discrimination; this criterion for absence of overt recognition is the same as that used in our work with P.H. [g, Task 71. Six faces of people famous in the 1960’s that met this criterion were spread out before MS. in a random 3 x 2 matrix, and he was twice instructed as to which name went with each face. Three faces were paired with true (correct) names; these were those of Tony Benn, Bobby Charlton and Ernie Wise. The other three faces (John Kennedy, Paul McCartney, Elvis Presley) were paired with untrue (exchanged) names (John Kennedy named as “Elvis Presley”, Elvis Presley identified as “Paul McCartney”, and Paul McCartney called “John Kennedy”). The test contained I2 trials, begun by rearranging the faces in the 3 x 2 matrix into a new order. M.S. was then asked to point to the paacecorresponding to a name that was given orally. If he made a mistake he was corrected. All six names were tested in a different order on each trial. Two days later, an equivalent test was given using six faces of people who have become famous since 1970. Faces of Jimmy Carter, Jack Nicholson and Norman Tebbit were paired with true (their own) names, and untrue (exchanged) pairings were created for the faces of Paul Daniels, Norman Fowler and Michael Parkinson.
Results. The number of times M.S. pointed to the correct face was separately determined for true pairings and for untrue pairings for each trial (max = 3 correct for any trial). Raw scores for 1960’s and post-1970 faces are shown in Table 3. Our method of analysing these data was the same as that used by DE HAAN et ul. [S] for similar learning tasks carried out with P.H. The sign test was used to compare performance with true and untrue pairings by scoring each trial as “+” (better on true than untrue pairings) “=” (equal performance with true and untrue pairings), or “ -” (better performance with untrue than true pairings). No difference was found either for 1960sfaces (3+ ,4=, S-, P>O.l) or for post-1970faces (5 +, 4=, 3-, P>O.l). Table 3. Numbers
of correct
choices
(max = 3) of face to match stated names on each trial of the face-name learning task (Task 2)
I 1960s faces Post-1970
faces
2
3
True pairings Untrue pairings
100020221213 002223123121
True pairings Untrue pairings
210312003222 2 110
4
5
11
Trial 6 I
8
9
2
2
11
10
11
12
2
1
184
FREDA NEWCOMBE. ANDREW W. YOUNG and EDWARD H. F. DE HAAN
Discussion. The results of this task provide no evidence ofcovert recognition for MS, either for faces of people famous before (1960s) or since (post-1970) his illness. Tasks 1 and 2 were thus consistent in finding that MS does not show covert recognition of familiar faces. In Tasks 3 and 4 we investigated whether he would show covert recognition of visually-presented objects.
OBJECT Tusk 3: Semantic
priming
RECOGNITION
of word recognition
The rationale for this task is similar to that of Task 1. MS. was asked to classify printed targetstimuliasbeingfamiliarwordsorpronounceablenonwords(lexicaldecision task).Each target was immediately preceded by a prime consisting of a photograph of an object presented for 500 msec. We were interested in determining whether or not the presence of a related object facilitated lexical decisions to target words. Facilitation of word recognition following presentation of related object primes is known to occur for normal subjects [19,21]. Stimuli and procedure. Two sets of 20 picture primes (photographs of objects) and word targets were created, such that each picture was of an object that was closely related to the word’s referent (e.g. a picture of a ring and the word “finger”, a picture of a nail and the word “hammer”). The words in these sets of related prime-target pairs were roughly matched for frequency. A list of the primes and targets from each set is given in Appendix 1. One set of prime-target pairs was then scrambled, so that the picture primes and word targets were Unrelated to each other, the other set was left to form the Related condition of the experiment. On each trial MS. was shown a back-projected picture prime for 500 msec, followed by a target word or a pronounceable nonword for 4 sec. Nonwords were created by changing one or two letters of nouns not used in the experiment. He was asked to decide as quickly and accurately as possible whether the target was a word or a nonword, and his reaction times (timed from target stimulus onset) were recorded from switches mounted in the vertical lever used to make his responses (with lever movement toward his body used to signal “word” responses, movement awayfrom his body for “nonword’responses). As for Experiment 1, MS. was told that each target would be preceded by a briefly presented stimulus, and was asked to look at this stimulus but make no response to it. The picture primes subtended visual angles of approx 6”. Eighty trials were run, involving the 20 Related picture-word pairs, the 20 Unrelated (scrambled) pairs, and 40 trials with a picture of a familiar object followed by a nonword target. These trials were arranged into an unpredictable order. At the end of the session MS. was shown all of the picture primes one at a time (with unlimited exposure), and asked to name them as quickly as possible. His response times were recorded using a voice key. The task was repeated a day later, but with the sets of stimuli used to create Related and Unrelated pairs reversed (i.e. the Related pairs from day 1became the Unrelated pairs for day 2). Six months later this entire procedure (both sessions) was repeated. The essential features of this design, then, are that MS. carried out a lexical decision task to target stimuli preceded by picture primes presented for 500 msec. These pictures were of objects that could be Related or Unrelated to target words.
Results. At the end of each of the four sessions, M.S. was tested for his ability to identify the primes used. He was able to identify a number of them, though his mean reaction time for those he could identify (i.e. name) correctly was 5095 msec. Table 4 summarizes his ability to identify the primes across these four sessions. For each prime we have calculated whether it was recognized on all four occasions, on three occasions, two occasions, one occasion, or not at all. Raw data are included in Appendix 1. Table 4 shows how the 40 primes used were distributed across these categories. It is clear that most primes were consistently recognized or consistently not recognized. A few primes (4) were, however, equally often recognized or not recognized; these were eliminated from consideration. The remaining primes were divided into 15 that were usually recognized (i.e. recognized on 3 or 4 occasions) and 21 that were usually not recognized (recognized on 0 or 1 occasions). Each of these primes had been used twice with a Related word and twice with an Unrelated
VISUAL
Table 4. Number
Number
RECOGNITION
of primes recognized
of primes
185
in 4, 3, 2, 1, or 0 of the four post-tests
4
Number 3
11
4
of times recognized 2 1 4
0
2
19
word across the four sessions. Thus mean reaction times could be calculated for correct responses to target words preceded by recognized or unrecognized primes in Related and Unrelated conditions. Mean reaction times for correct responses to word targets preceded by recognized or unrecognized primes are shown in Table 5. M.S. made few errors in the lexical decision task (overall error rate < 2%). His mean reaction time for “nonword” responses was 1890 msec.
Table 5. Mean reaction times (in msec) for correct responses to target words preceded by Related or Unrelated picture primes that M.S. could or could not identify in the post-test
Prime recognized (A’= 15) Prime not recognized (N=21)
Related
Unrelated
1329 1600
1717 1.585
An unequal cells analysis of variance of the correct reaction times to word targets was carried out to determine the effects of prime Type (Related or Unrelated; repeated measure) and prime Recognition (prime usually recognized or not usually recognized in the post-test). There was no overall difference in reaction times to target words preceded by recognized or unrecognized primes (F-C l), and the main effect of prime Type did not reach statistical significance [F (1, 34)=3.15, O.l> P>O.O5]. There was, however, a significant prime Type x prime Recognition interaction [F (1, 34) = 5.31, PC O.OS], Tukey tests (X = 0.05) showed that responses for words preceded by Related primes that M.S. could recognize in the post-test were faster than responses in the other three cells of the analysis, which did not differ from each other. Discussion. The analysis of potential covert effects in object recognition tasks is complicated by the fact that M.S. is able to identify a substantial proportion of presented objects. Once the picture primes are separated into those he can and cannot usually recognize, however, it is clear that semantic priming was only obtained for primes that M.S. could overtly identify. Hence, as for faces, there is no evidence of covert recognition of objects he cannot identify. It is interesting, though, that M.S.‘s reaction times for overt identification should be so long (5095 msec) when the priming effect can be shown to a 500 msec presentation. We suspect that part of the reason for his long reaction times for overt identification reflects caution created by loss of confidence in his own visual recognition abilities. Because of constraints on the number of photographs of objects available to us when Task 3 was constructed, a Neutral prime condition was not included. Since there was no evidence of priming from unrecognized objects, however, these might themselves be considered to form a Neutral condition. The fact that reaction times for target words
186
FKEDA NEWCOMLIE,ANDKEW W. YOUNG and EDV~AKDH. F. DE HAAPG
preceded by Related primes that M.S. could recognize were faster than reaction times in the remaining three word target conditions (which did not differ from each other) would then indicate that the semantic priming effect from pictures he can recognize is one of facilitation without inhibition. The results of Task 3, then, imply that M.S. does not show covert recognition of objects he is unable to identify overtly. In order to confirm this conclusion by a different method, Task 4 employed an object matching task. Task 4: Object matching
M.S. is able to match photographs to determine whether they show same or different objects, provided that the difference in views is not too extreme. We thus decided to investigate whether or not he would be able to match views of unrecognized familiar objects more quickly than he could match views of unfamiliar objects. The logic of this procedure is the same as that used for face matching tasks by DE HAAN et al. [S, Tasks 1 and 21; covert recognition would produce faster matching of unrecognized familiar objects than unfamiliar objects. Stimuli and procedure. Two photographs were taken of each of 53 familiar everyday objects and 53 unfamiliar objects. The 53 unfamiliar objects represented as many as we could find after a fairly diligent search; they included pieces of hospital and laboratory equipment, machine fittings. obscure car spares, parts of broken household utensils, unusual electrical fittings, and so on. All of these unfamiliar objects achieved a very low mean familiarity in a set of ratings made by six normal people of M.S.‘s age. Photographs were taken from a range of angles, with no attempt to standardize these: we relied instead on the sheer number of pairs to control for differences in camera angle. Slides ofthese object photographs were presented (back-projected) to MS. in pairs, with one positioned vertically above the other. Examples of “same” pairs of famihar and unfamiliar objects are shown in Fig. I. Each of the 53 familiar pairs and 53 unfamiliar pairs was presented once in the course of the experiment, and each of these photographs was also used once as a member of a pair of photographs of different objects. Each pair of photographs was presented for 4 set, and MS. was asked to decide whether or not they showed same or different objects. Responses (timed from stimulus onset) were made using the lever mechanism already described (with movement toward his body used to signal “same”, and away from his body to signal “different”). “Same” and “different” pairs, and pairs involving familiar or unfamiliar objects, were arranged into random order. The experiment was divided into two separate sessions, with a 6-month interval in between. At the end of each session MS. was shown all the stimuli that had been used in that session with unlimited presentation time. and asked to identify (i.e. name) the objects in the “same” pairs.
Results. Only reaction times to “‘same” pairs were analysed. It is possible to separate reaction times to the “same” pairs into those to objects which M.S. could or could not recognize in the test of overt recognition given at the end of each experimental session. This cannot be done for responses to “different” pairs where M.S. may recognize either, both or neither of the objects. His mean reaction times for correct responses to different pairs were 2075 msec for familiar pairs and 2186 msec for unfamiliar pairs, with 52/53 responses correct to each type of pair. Reaction times to “same” pairs were separated for analysis into those to familiar objects that were or were not recognized in the post-test, and those to unfamiliar objects. Mean correct reaction times are presented in Table 6. The MannWhitney U-test was used to compare reaction times to recognized and not recognized familiar pairs, showing that the objects which could be recognized on the post-test were matched more quickly (nI =23, n2 =28, lJ=430.5, ~=2.05, 2-tailed P~0.05). There was, however, no difference between reaction times for familiar pairs which could not be recognized and unfamiliar pairs (trl = 28, n,=49, U=812, z= 1.33, 2-tailed P>O.l).
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FAMILIAR FIG. 1. Examples
187
UNFAMILIAR of “same” pairs of familiar
and unfamiliar
objects (Task 4).
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189
Table 6. Mean correct reaction times (in msec) for correct matching of “same” pairs of familiar objects that were or were not recognized in the post test, and “same” pairs of unfamiliar objects (Task 4) Familiar
objects
Recognized
Not recognized
Unfamiliar objects
1886 N=23
2401 N=28
2529 N=49
Discussion. As for Task 3, there is no evidence of covert recognition. Instead, it is clear that MS. is only better able to match views of familiar objects that he can recognize overtly. GENERAL
DISCUSSION
Our findings point consistently to the same conclusion; MS. does not show covert recognition. In Task 1 semantic priming of name recognition was obtained from name primes but not from face primes. In Task 2 M.S. showed no advantage for learning true rather than untrue face-name pairings, both for faces of people famous before his illness and for faces of people who have become famous since he was ill. In Task 3 semantic priming of lexical decision was obtained only from picture primes that MS. was able to recognize overtly. In Task 4 faster matching of “same” pairs of photographs of familiar than unfamiliar objects was again found only for objects that M.S. could recognize overtly. For MS.. then, his ability to recognize faces and objects is much the same whether it is tested with tasks demanding implicit or explicit recognition. M.S.‘s performance is thus different to that of the patient P.H. [S], w”lo showed evidence of ability to recognize familiar faces on implicit but not on explicit tasks. This finding of a difference between M.S. and P.H. is particularly interesting because on tests of overt face recognition ability there is no apparent difference between P.H. and M.S. (see Table 1); both are unable to recognize familiar faces overtly. But the pattern of covert recognition effects shown by P.H. on implicit tests is not found for MS. It seems unlikely that the difference in elapsed time since injury might be important in accounting for the presence or absence of covert recognition in M.S. and P.H. We investigated P.H.‘s covert recognition abilities some 5 to 6 yr after his accident, whereas the present work with MS. has been conducted some 16 to 17 yr after his illness. One could perhaps speculate that covert recognition effects might simply die away once overt recognition is no longer possible. However, the 5-6 yr interval between P.H.‘s injury and our testing sessions is itself considerable, yet we were able to demonstrate that P.H. showed covert recognition even to faces of people he had only met since his accident [S]. Thus for P.H. there is no sign of covert recognition tailing off, and it is found even for faces he has never been able to recognize overtly. The difference between M.S. and P.H. that we consider crucial is that M.S. shows more obvious signs of higher-order perceptual impairment. He has a marked object agnosia, and performs very poorly on face matching tasks. P.H. is himself not completely free from problems in object recognition and face matching tasks, but his difficulties do not approach the severity of those experienced by M.S.; M.S. is clearly agnosic in daily life, whereas P.H.‘s problems with object recognition show up only in formal tests. The existence of higher-order
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FREDA NEWCOMBE.ANDREWW. YOUNG and EDWARDH. F. DE HAAN
perceptual impairment for M.S. means that he is probably unable to construct visual representations adequate for the recognition of faces and many everyday objects. In BRUCE and YOUNG’S [S] terms MS’s impairment affects structural encoding. Without adequate structural encoding neither overt nor covert recognition will be possible. This conclusion is consistent with BAUER’S[3] failure to find evidence ofcovert recognition offamiliar faces in the skin conductance responses of the patient G.Y ., who had a marked apperceptive impairment. The differences between MS. and P.H., then, are consistent with the distinction between perceptual and mnestic forms of prosopagnosia emphasized by DE RENZI [9]. It is thus possible that presence or absence of covert recognition of familiar faces will provide an additional index of these contrasting types of face recognition impairment.
REFERENCES I. BAUER, D. W. and STANOVICH, K. E. Lexical access and the spelling-to-sound regularity effect. Memory Cognition, 8, 424432, 1980. 2. BAIJER, R. M. Autonomic recognition ofnamesand facesin prosopagnosia: a neuropsych0logical app!ication 3. 4. 5. 6. 7. 8. 9. IO.
II. 12. 13.
14. 15. 16. 17. 18.
IY. 20. 21, 22. 23. 24.
und
of the guilty knowledge test. Neuropsychologia 22,457469, 1984. BAUER, R. M. The cognitive psychophysiology of prosopagnosia. In Aspects of Face Processing, H. D. ELLIS,M. A. JEEVES,F. NEWCOMLIEand A. YOUNG (Editors), pp. 253%267. Martinus Nijhoff, Dordrecht, 1986. BOUAMER,J. Die Prosop-Agnosie. Archiv Jk Psychiatric und Nervenkrankheiten 179, 6&53, 1947. BRUCE, V. and YOUNG, A. W. Understanding face recognition. Br. J. Psychol. 77, 305-327, 1986. DAMASIO, A. R., DAMASIO, H. and VAN HOESEN, G. W. Prosopagnosia: anatomic basis and behavioral mechanisms. Neurology 32, 331-341, 1982. DE HAAN, E. H. F., YOUNG, A. and NEWCOMBE,F. Faces interfere with name classification in a prosopagnosic patient. Cortex 23, 309 316, 1987a. DE HAAN, E. H. F., YOUNG, A. and NEWCOMBE,F. Face recognition without awareness. Cognir. Neuropsychol. 4, 385-415, 1987b. DE RENZI, E. Current issues in prosopagnosia. In Aspects of face Processing, H. D. ELLIS, M. A. JEEVES, F. NEWCOMBEand A. YOUXG (Editors), pp. 243- 252. Martinus Nijhoff, Dordrecht, 1986. H~(.AEN, H. The neuropsychology of face recognition. In Perceiving and Remembering Fuces, Cr. DAVIES, H. ELLIS and J. SHEPHERD (Editors). pp. 39-53. Academic Press, New York, 1981. H&AEN, H. and ANGELERGLXS,R. Agnosia for faces (prosopagnosia). Arch.? Neural. 7, 92- 100. 1962. MEADOWS, J. C. The anatomical basis of prosopagnosia. J. Naurol. Nettrosurg. Psychiut. 37, 489-501, 1974. NEWCOMBE,F. and RATCLIFF, G. Agnosia: a disorder of object recognition. In Les Syndromes de Disconnexion Culleuse chez /‘Hornme, F. M~CHEL and B. SCHOTT (Editors), pp. 317--341. Colloque International de Lyon, Lyon, 1975. POSNFR, M. I. and SNYL)EK,C. R. R. Facililation and inhibition in the processing of signals. In Artrntion and Pwformance. P. M. A. RABBITT and S. DORNIC (Editors), pp. 669-682. Academic Press, London, 1975. RAYTLIFFE,G. and NEWTOMBE,F. Object recognition: some deductions from the clinical evidence. In Normalit) and Pathology in Cognitive Functions. A. W. ELLIS (Editor). pp. 147- 171. Academic Press, London, 1982. SAE~RAN, E. M. and MAWIN. 0. S. M. Reading without phonology: evidence from aphasia. Q. /. e.up. Psycho/. 29, 515 -525, 1977. SctlACTER, D. L. Implicit memory: history and current status. J. esp. Psychol.: Lrurn. k/em. (‘ognil. 13, 501 518, 1987. SCHACTFR, D. L., MCANDREWS, M. P. and Mos~(>vIT(.H. M. Access to consciousness: dissociations between implicit and explicit knowledge in neuropsychological syndromes. In Thouqhl Withour Lunyuaye, I.. WEISKKANTZ (Editor). Oxford University Press, Oxford, 1988. SPERRER, R. D., MTCAULEY, C., RAGAIN. R. D. and WFIL, C. M. Seman!ic priming effects on picture and word processing. Mem. Coynil. 7, 339-345, 1979. TRANEL, D. and DAMASIO, A. R. Knowledge without awareness: an autonomic index of facial recognition by prosopagnosics. Science 228, 1453-1454, 1985. VAtJDERwART. M. Priming by pictures in lexical decision. J. oerh. Learn. verb. Behap. 23, h7- 83, 1984. YOUNG, A. W. and DE HAAN, E. H. F. Boundaries of covert recognition in prosopagnosia. Cognil. Neuropsychol. 5, 317-336, 1988. YOUNG, A. W., HAY, D. C.. MCWEENY, K. H., FLUDE, 8. M. and ELLIS, A. W. Matching familiar and unfamiliar faces on internal and external features. Perception 14, 737-746. 1985. YOUNG, A. W., H~LLAWLLL, D. and DE HAAN, E. Cross-domain semantic priming in normal subjects and a prosopagnosic patient. Q. J. ewp. Psycho/. 40A, 1988.
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APPENDIX
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1
List of picture primes and word targets used in Task 3. Numbers in brackets indicate the number (max = 4) MS. was able to identify each prime overtly in the four post-test sessions Set
1
Picture Pushchair Bread Vacuum cleaner Clothes peg Paint Mirror Shoes Camera Matches Lawnmower Shears Watch Rake Crash helmet Safety pin Violin Boat Aeroplane Envelope Tennis ball
Set 2 Word
(2) (0) (0) (0) (0) (2) (4) (3) (0) (0) (1) (4) (0) (0) (0) (0) (0) (4) (4) (0)
Butter Carpet Clothes Door Face Feet Film Fire Grass Hedge Hour Leaves Motorcycle Nappy Orchestra Sea Sky Stamp Tennis
Word
Picture Trumpet Head Biscuits Pie Kettle Glasses Ring Comb Lipstick Hammer Pencil Scissors Bed Car Frying pan Iron IJmbrella Bucket Track shoes Grapes
;:I (3) (0) (2) (4) (2) (4) 1:; (4) (4) (0) (3) (0) (0) (4) (1) (4) (0)
Band Body Cheese Chips Coffee Eyes Finger Hair Mouth Nail Paper Paste Pyjamas Road Sausages Shirt Shower Spade Sport Wine
of times