intact recognition of emotional prosody following amygdala damage

Intact recognition of emotional prosody following amygdaladamage

Ralph Adolphs*, Daniel Tranel

Department of Neurology, Division of Cognitive Neuroscience, University of Iowa College of Medicine, Iowa City, Iowa, USA

Received 20 July 1998; accepted 4 January 1999

Abstract

Bilateral damage to the amygdala in a variety of animal species can impair emotional reactions to stimuli in several sensory

modalities. Such damage in humans impairs visual recognition of emotion in facial expressions, but possible impairments inmodalities other than vision have not been su�ciently explored. We examined two subjects with complete bilateral amygdaladamage, and seven with unilateral amygdala damage, on a standardized task of emotional prosody recognition. The data were

compared to those from 15 brain-damaged and from 14 normal control subjects. One of the bilateral amygdala subjects, whoselesions were restricted to the amygdala, was entirely normal in recognizing emotion in prosody on all tasks; the other, whosedamage included substantial lesions also in extra-amygdalar structures, especially in right hemisphere, was normal on most,

albeit not all, measures of emotional prosody recognition. We suggest that the human amygdala's role in recognizing emotion inprosody may not be as critical as it is for facial expressions, and that extra-amygdalar structures in right hemisphere may bemore important for recognizing emotional prosody. It remains possible that recognition of emotion in classes of auditory stimuli

other than prosody will require the amygdala. # 1999 Elsevier Science Ltd. All rights reserved.

Keywords: Emotion; Fear; Auditory; Human; Lesion

1. Introduction

The amygdala receives highly processed sensoryinput from all sensory modalities, and direct olfactoryinput from the olfactory bulb [1]. It projects both toneocortex as well as to limbic structures and hypo-thalamus, making it an ideal candidate for partici-pation in the processes that link sensory perception toemotional response. A large number of studies in ani-mals has con®rmed the amygdala's role in processingemotionally signi®cant stimuli in multiple sensorymodalities [2±11].

The connectivity and anatomy of the primate amyg-dala are notable for an exceptionally large input fromvisual cortices, and a corresponding increase in the size

of the basolateral amygdala, which receives such input

[1,12]. Projections from the amygdala back to visual

cortices are also more prominent in primates than in

other species, including direct projections to all tem-

poral visual cortices as well as to V1 [13]. While the

amygdala receives a direct projection from parts of the

auditory thalamus involved in acoustic fear-condition-

ing, its connections with auditory cortices are less well

understood.

A number of lesion [14±18] and functional imaging

studies [19,20] in humans have con®rmed the amygda-

la's critical role in recognizing emotional facial ex-

pressions, notably fear. Furthermore, activity within

the amygdala during the recognition of emotional

facial expressions correlates with activity in visual cor-

tices [21]. However, investigations of the human amyg-

dala's role in processing emotions signaled by stimuli

in other sensory modalities has only just begun.

In regard to the auditory modality, one recent case

study reported impaired recognition of emotional pro-

Neuropsychologia 37 (1999) 1285±1292

0028-3932/99/$ - see front matter # 1999 Elsevier Science Ltd. All rights reserved.

PII: S0028-3932(99 )00023 -8

www.elsevier.com/locate/neuropsychologia

* Corresponding author. Department of Neurology, University

Hospitals and Clinics, 200 Hawkins Drive, Iowa City, IA 52242,

USA. Tel.: +1-319-356-4296; fax: +1-319-353-6277.

E-mail address: [email protected] (R. Adolphs)

sody following partial and non-selective bilateraldamage to the amygdala for the treatment of epilepsy[22], whereas another case study with bilateral damagemore restricted to the amygdala found no such impair-ment [23]. One functional imaging study to date hasreported amygdala activation in response to emotionalauditory stimuli [24]. A possible explanation for thediscrepant ®ndings may be that the impairments thathave been reported [22] are due not to amygdaladamage, but instead resulted from damage to the rightbasal ganglia (see [23] for discussion). On the otherhand, neither of these case studies [22,23] had completedamage to the amygdala, and it is conceivable that theimpaired subject had lesions to some portions of theamygdala that may have been spared in the other sub-ject.

Given the limited number of con¯icting reportsreviewed above, it was important to replicate ®ndingsin additional cases, and to compare performances witha group of brain-damaged controls. Of special interestwas an investigation of subject SM046, who provides acase of bilateral damage to the amygdala that is bothcomplete and selective, making this subject ideal fortesting the hypothesis that emotional prosody recog-

nition requires at least some portion of the amygdala.SM046 has been well described in regard to herimpaired recognition of emotional and social infor-mation from faces [14,15,25,26], but her recognition ofemotional auditory stimuli is reported here for the ®rsttime.

To explore the human amygdala's role in recog-nition of emotion in auditory stimuli, we testedSM046, and another subject with complete but non-selective amygdala damage, on their recognition ofemotion in prosody. We also included seven subjectswith unilateral amygdala damage. To facilitate com-parison, we used an auditory recognition task identicalin protocol to the task we have previously used todemonstrate impaired recognition of emotion in facialexpressions. Subjects were asked to judge the intensityof emotion displayed in human voices reading semanti-cally neutral sentences. Fifteen brain-damaged subjectswithout damage to amygdala, and fourteen normalsubjects, served as controls.

As noted above, the studies available thus far havereached somewhat discrepant conclusions. Since thecase reported by Anderson and Phelps [23] (who hadnormal recognition of emotional prosody) is consider-

Table 1

Demographics and neuropsychology

Subjecta Gender Age VIQ PIQ Facial emotion Prosody Lesionc

Bilateral SM046 F 30 86 90 Impaired Normal Complete

RH1951 M 42 110 116 Impaired Normal Complete

Right SB1932 F 35 91 96 Normal Normal 50%

AK1603 F 25 106 133 Normal Impaired 100%

Left LV580 F 31 81 112 Normal Normal 100%

JS1077 M 22 129 126 Normal Normal 50%

UB1251 M 35 93 99 Normal Normal 100%

CS1404 M 23 114 108 Normal Normal 75%

MA2023 M 34 102 110 Normal Normal 100%

B.D. control LP194 F 48 84 92 Normal Impaired L Parietal

JG468 M 68 111 132 Impaired Impaired L Frontal

VY500 F 66 113 88 Normal Normal B Frontal

DM1045 F 43 95 105 ± Normal L Occipital

AH1331 M 62 117 95 Normal Impaired R Frontal

RJ1374 M 52 96 96 Normal Normal R Occipital

JR1584 M 51 90 111 Normal Impaired B Frontal

CG1652 M 42 101 102 Impaired Normal L Frontal

GG1656 M 51 93 105 Normal Normal L Parietotemporal

BL1722 F 52 85 85 Normal Normal B Hippocampal

AR1730 M 58 96 109 Normal Normal R Parietal

WH1737 M 60 117 95 Normal Normal R Occipitotemporal

MR1790 F 62 97 80 Normal Impaired R Occip.+L Frontal

RR1962 M 66 (a)b 141 Normal Normal L Parietotemporal

SA2081 M 38 120 98 Normal Normal L Parietal

a Subject ID from the Patient Registry. Bold indicates subjects with bilateral lesions. VIQ, PIQ: verbal and performance IQ from the WAIS-R.

Facial Emotion, Prosody: recognition of emotion in facial expressions or from prosody. For both facial emotion and emotional prosody, r< 0.5

was labeled `impaired'.b (a): subject was severely aphasic.c For subjects with amygdala damage, volumetric extent of damage was classi®ed in three categories (25±75% denoted by `50%'; 50±100%

denoted by `75%', or complete denoted by `100%'). For controls, side and regional location is given.

R. Adolphs, D. Tranel / Neuropsychologia 37 (1999) 1285±12921286

ably more similar to our subject SM046 in terms ofhaving selective and bilateral amygdala damage, wehypothesized that SM046 would have normal recog-nition of emotional prosody.

2. Methods

2.1. Subjects

We studied two subjects with complete bilateralamygdala damage, two with unilateral right amygdaladamage, ®ve with unilateral left amygdala damage,and 15 brain-damaged controls without damage toamygdala. All brain-damaged subjects were screenedwith a standard audiometry task, and none showedany signi®cant hearing loss at any frequency. Datafrom brain-damaged subjects were compared to thosefrom 14 normal controls (seven male, seven female;age=52216). Background demographic and neurop-sychological data are given in Table 1. All brain-damaged subjects were selected from the PatientRegistry of the Division of Behavioral Neurology andCognitive Neuroscience at the University of Iowa, andhad been fully characterized neuroanatomically [27,28]and neuropsychologically [29]. All subjects gaveinformed consent to participate in these studies, in ac-cordance with a protocol approved by the HumanSubjects Committee of the University of Iowa.

2.2. Subjects with bilateral amygdala lesions

Subject SM046 is a 31-year-old woman with a high-school education who has focal bilateral amygdaladamage resulting from Urbach-Wiethe disease[14,15,30,31], a hereditary illness. Detailed neuroanato-mical analysis indicates that she has complete lesionsof both amygdalae, but no damage to more distantstructures.

Subject RH1951 had Herpes simplex encephalitis atage 28. He has no history of neurological or psychia-tric disease prior to the encephalitis. RH1951 has com-plete bilateral destruction of the amygdala andsubstantial damage to surrounding structures, as istypical of Herpes simplex encephalitis. His damage isespecially extensive on the right, including largeregions of temporal cortex. He is severely amnesic.The extent of lesions in SM046 and RH1951 wasdetermined by detailed examination of 3-dimensionalreconstructions of their brains from MR scans [28,32].

2.3. Subjects with unilateral amygdala lesions

All subjects with unilateral amygdala lesions hadsurgical temporal lobectomy for the treatment of epi-lepsy. All these subjects also had some degree of uni-

lateral damage to hippocampus and surroundingtemporal cortices. The extent of their amygdaladamage is given in Table 1.

2.4. Brain-damaged controls

Fifteen control subjects with brain damage outsidethe amygdala included subjects with lesions in parietal,temporal, frontal, and occipital cortices. Several of thesubjects had bilateral lesions (cf. Table 1). The brain-damaged controls were an initial, random sample ofsubjects with cortical lesions, of whom we have nowtested over 60 with respect to their emotional prosodyrecognition. A more detailed investigation of thee�ects of cortical lesions on emotional prosody recog-nition will be presented with this larger subject samplein a future report (cf. Discussion).

2.5. Background auditory perception and recognitiontasks

2.5.1. AudiometryWe assessed basic auditory acuity as a function of

frequency, by measuring monaural hearing thresholdsfor tones (250, 500, 750, 1000, 1500, 2000, 4000, 6000,8000 Hz) with a calibrated audiometer (model MA25,Maico Hearing Instruments, Minneapolis, MN).

2.5.2. Environmental sound recognitionComplex auditory recognition was assessed by

administering 100 various environmental sounds,including sounds of machinery, animals, musicalinstruments, and people, according to a standardizedprotocol. Brie¯y, correct recognition was operationa-lized as the ability to give information su�cient tounambiguously identify the stimulus; while correctnaming necessarily entailed correct recognition, therewere several instances of correct recognition withoutnaming (see [33] for details of the protocol and scoringmethods used).

2.6. Experimental task

We carefully designed our stimuli so that they onlyvaried with respect to a single factor of interest:emotional prosody. We used sentences spoken by ahuman performer instructed to produce a speci®cemotional tone of voice, the type of stimulus mostcommonly used to assess prosody recognition on bothnormal and brain-damaged human subjects [23,34±37].The same four semantically neutral English sentenceswere spoken by the same female voice for each of ®vedi�erent prosodic emotions: happiness, sadness, anger,fear, surprise, and also for neutral and sleepiness. Weexcluded prosodic stimuli denoting disgust, as thisemotion was highly ambiguous to signal with prosody

R. Adolphs, D. Tranel / Neuropsychologia 37 (1999) 1285±1292 1287

alone, resulting in a large variance even in normal sub-jects. The total of 28 sentences were recorded, digi-tized, and normalized for average amplitude to avoidthe possibility that subjects could deduce the correctemotion simply by reasoning from perceived loudness.Sentences were played in randomized order to subjectsat a level they indicated was su�ciently loud. Each

sentence had a duration of approximately 3 seconds,with a 10 s interstimulus interval. All stimuli were pre-sented in free ®eld.

Subjects heard the 28 sentences 8 times, and ratedthem on a scale of 0 (=`not at all') to 5 (=`verymuch') with respect to the labels, àwake', `happy',`sleepy', `sad', àngry', àfraid', `disgusted', `surprised'.

Table 2

Normal ratings of emotional prosodya

Label Happy Sleepy Sad Disgusted Angry Scared Surprised

Prosody

Happy 3.220.7 0.620.7 0.620.6 0.620.7 0.420.6 0.420.5 1.620.9

Sad 0.320.6 2.221.2 3.820.5 1.621.4 1.121.2 1.721.5 0.920.9

Angry 0.820.7 0.420.5 1.621.3 3.220.9 3.520.7 0.921.1 0.920.9

Afraid 1.321.1 0.820.9 1.821.2 0.921.0 1.020.9 2.821.2 2.521.2

Surprised 2.421.4 0.520.7 0.720.8 0.620.9 0.420.5 0.620.6 3.720.8

a Means and S.D. of ratings given by 14 normal controls. Bold indicates the highest rating given to stimuli of that emotion category.

Fig. 1. Mean ratings of the intensity of emotion expressed by prototypical prosodic stimuli. Means are shown for the four stimuli within each

emotion category. Grey bars indicate means and S.D. given by 14 normal controls. (a) Means given by each of 15 brain-damaged controls (r);

(b) means given by two subjects with complete bilateral amygdala damage (SM046, w, three experiments; and RH1951, q, one experiment), and

by two subjects with unilateral right (Y) and ®ve with unilateral left (U) amygdala damage.


This procedure was identical to the one we have pre-viously used with visual stimuli of emotional facial ex-pressions [14,15,38].

2.7. Data analysis

Data were analyzed in three ways: (1) we calculatedmean ratings given to the four stimuli of each emotioncategory when rating with respect to the label thatdenoted the intended emotion (e.g., the mean ratinggiven to the four happy prosodic stimuli on the label`happy'); (2) we determined the label amongst the sixemotions which had received the highest rating as cor-responding to the emotion label that best described theface; (3) we correlated the ratings given to each stimu-lus on all the eight labels with the ratings given bynormal controls. The ®rst measure describes the inten-sity of the prototypical emotion subjects judged eachstimulus to depict and gives an index of the sensitivityto that particular emotion. The second measure deter-mines the emotion label judged to be maximallyintense for that face; this derived measure provides aclose comparison with respect to the data of Scott etal. [22], who obtained such data directly from a six-alternative forced-choice labeling task. The thirdmeasure describes the entire range of emotions judgedfor each stimulus, and is not subject to ceiling or ¯oore�ects. We have published our ®ndings with emotionalfacial expressions using both analyses 1 and 3[14,15,38]; all three analyses have been used in otherstudies of emotional prosody [22,23].

3. Results

Background neuropsychological data are given inTable 1. Of relevance is the previously reported ®ndingthat subjects with bilateral amygdala damage areimpaired in recognizing emotional facial expressions,especially fear [14,15]. Both subjects with bilateralamygdala damage, SM046 and RH1951, had normal

hearing thresholds at all frequencies as determined byaudiometric testing, and both had normal recognitionof environmental sounds (SM046: 92% correct;RH1951: 89% correct; normal controls: 9223% cor-rect).

3.1. Judging the intensity of emotion expressed by voice

Normal subjects gave prosodic stimuli the highestrating on the label of the emotion that the stimuluswas intended to express (Table 2). As with facial ex-pressions of emotion [14,39,40], fear tended to besomewhat confused with surprise, and anger with dis-gust, providing further evidence that these emotionconcepts have considerable overlap.

Subjects with either unilateral or bilateral amygdaladamage rated the intensity of each prototypicalemotion expressed in prosody within 2 S.D. of themean ratings given by normal controls, similar or bet-ter than the performance of brain-damaged controls(Fig. 1). While there was a considerable range in theratings given, and a fair degree of variance in normalratings, there was no evidence that subjects with bilat-eral amygdala damage were impaired on this measure.Particularly striking were the data from 3 experimentswith SM046 (circles in Fig. 1), who performed within1 S.D. of normal control ratings on all emotions,including fear, an emotion which she cannot recognizein facial expressions.

The above raw data show a relatively large variance,due to di�erent subjects having di�erent judgmentsabout how `intense' a given numerical rating shouldbe. We derived two measures from the raw data thatcontrol for subjects' di�erent general biases in thisregard.

3.2. Derivation of best label

From each subject's ratings for each stimulus, wedetermined the maximal rating given to any of the sixemotion labels. While such a derived measure is not

Table 3

Best label for each emotiona

Emotion RH1951 SM046 Unilateral BDC:avg BDC:SD NC:avg NC:SD

Happiness 1 1 1.00 0.82 0.28 0.91 0.12

Sadness 0.75b 1 0.89b 0.85b 0.25 0.98 0.07

Anger 0.75 1 0.93 0.71 0.24 0.89 0.23

Fear 0.25b 0.5 0.68 0.52 0.29 0.64 0.32

Surprise 1 0.5 0.89 0.91 0.16 0.89 0.27

a For each face stimulus, the best choice of label was derived by picking that label which had received the maximal intensity rating. When the

maximal label corresponded to the single correct emotion label for that face, a score of 1 was given; maximal labels that did not correspond to

the single correct emotion received a score of 0. Means and S.D. are shown for normal controls (NC), for brain-damaged controls (BDC), and

for subjects with amygdala damage.b Scores <1 SD below NC mean.


identical to the direct measure obtained from a six-alternative forced-choice task, it provides the bestcomparison with such a task. These derived measuresare presented in Table 3. Subjects with amygdaladamage were no less accurate on this measure of thebest emotion label than were brain-damaged controls.While SM046's derived best labels were within thenormal range, it is interesting to note that RH1951'sderived best labels were impaired in regard to fear(as he tended to mislabel fear as surprise or happi-ness).

3.3. Correlations of ratings with normal ratings

As a further derived measure that gets around theproblem of potential ¯oor or ceiling e�ects when rat-ing the intensity of prototypical emotions, we corre-lated the ratings given to a stimulus on all eightemotion labels with ratings given to that stimulus bynormal controls. Such correlational measures havebeen widely used in research on emotion recognition[14,15,39,40], and provide a sensitive measure of poss-ible impairment. In general, subjects with amygdaladamage gave ratings that correlated highly with nor-mal ratings (Fig. 2). Speci®cally, SM046 gave ratingsthat correlated with normal ratings at better than2 S.D. above the mean normal correlation for everyemotion (Fig. 2b). RH1951 fell somewhat below nor-mal correlation with respect to anger, and one of thetwo subjects with unilateral, non-selective, right amyg-dala damage, AK1603, was impaired with respect tofear. Interestingly, several of the brain-damaged con-trols, who did not have any damage to amygdala, wereimpaired on the task (Fig. 2 and Table 1). While theprecise regions within which lesions can impair recog-nition of emotional prosody will be the topic of afuture study from our group, the data from the brain-damaged subjects we include in the present paperdemonstrate that damage to sites outside the amygdalacan result in severe impairment in recognition ofemotional prosody. This makes it especially importantto control for possible extra-amygdalar damage wheninvestigating the amygdala's contribution to this func-tion, an issue we take up in more detail in theDiscussion.

4. Discussion

We used here a procedure identical to the one withwhich we have previously demonstrated impairmentsin the recognition of emotional facial expressions. Thepresent ®ndings demonstrate that bilateral damage tothe human amygdala does not necessarily impair rec-ognition of emotion in prosody. Both SM046 andRH1951 are impaired in recognizing emotional facialexpressions, yet neither subject was impaired in recog-nition of emotion in prosody, with the possible excep-tion of RH1951's performance on a derived labelingmeasure (see below). The data are especially strikingfor SM046, who was severely impaired in recognizingfearful facial expressions in four replications of an ex-periment [14,15], but entirely normal in recognizing allemotions from prosody in three replications in the pre-sent study.

One possible explanation for these ®ndings could bethat it is simply easier to recognize emotion in prosodythan in facial expressions. Clear evidence against this

Fig. 2. Correlation of subjects' ratings with the mean ratings given

by normal controls. (a) Correlation of ratings given by brain-

damaged controls (r). Grey squares indicate means and S.D. given

by 14 normal controls (each normal control's ratings were correlated

with the mean ratings of the remaining 13 for this analysis); (b) cor-

relation of ratings given by two subjects with complete bilateral

amygdala damage (SM046, w, three experiments; and RH1951, q,

one experiment), and by two subjects with unilateral right (Y) and

®ve with unilateral left (U) amygdala damage. Grey bars denote

2 S.D. below the mean of the 14 normal controls.


account comes from normal subjects' performances: asTable 2 and the ®gures show, we did not have ceilinge�ects for the stimuli, especially in regard to negativeemotions, which were not trivial to recognize even fornormal subjects. It is thus all the more striking thatsubjects with bilateral amygdala damage performednormally on the task.

Another strong argument against the possibility thatdi�culty alone could account for impaired recognitionof emotion in either facial expressions or in prosody isthe presence of double dissociations. SM046 wasclearly impaired in recognizing emotion in facial ex-pressions, but not in prosody. Conversely, severalbrain-damaged controls were severely impaired inrecognizing emotion in prosody, but entirely normalwhen judging facial expressions. The presence ofdouble dissociations clearly indicates that level of di�-culty alone cannot account for the current ®ndings.

Several studies have reported impairments in recog-nizing emotional prosody following damage to righthemisphere [34±38,41,42], and functional imaging stu-dies have shown activation of right hemisphere struc-tures when recognizing emotional prosody [43]. Allthese studies are consistent with the hypothesis thatcortices in right hemisphere may have a relativespecialization to process the emotional signi®cance ofauditory stimuli. In a study that is still in progress, wehave tested over 60 subjects with cortical lesions on atask identical to the one used in the present study, andfound unequivocal evidence that lesions in right corti-cal regions impair recognition of emotion in prosody.The details of this study will be reported elsewhere,but they corroborate the importance of structuresother than the amygdala in recognizing emotional pro-sody.

A ®nal issue concerns how to reconcile our ®ndingswith those of Scott et al. [22], who reported impairedrecognition of emotion in prosody, together with otherauditory recognition impairments, in a subject (D.R.)whose amygdala had been surgically lesioned to con-trol epilepsy. While both the stimuli and procedureused by Scott et al. di�ered from the ones we used inthe present study, a comparison can be made betweenthe data of Scott et al. [22] and our Table 3, whichpresents a similar derived measure. With this analysis,one of our subjects with bilateral amygdala damage(RH1951) was indeed impaired in recognizing fear.RH1951 also gave a borderline impaired performanceon the correlational measure in regard to fear, as didone of the subjects with unilateral right temporallobectomy (AK1603; Fig. 2). SM046, however, wasnot impaired on any of these measures with respect toany emotion. As RH1951 (as well as subject AK1603)di�er from SM046 in that there is much more exten-sive damage to temporal lobe structures, especially onthe right (whereas SM046 has damage con®ned to

amygdala), these ®ndings raise the possibility that the®ndings of Scott et al. [22] might also be due todamage to structures other than the amygdala. Indeed,Scott et al. report some damage to extra-amygdalarstructures visible in MR scans, notably the right basalganglia.

These considerations leave open the possibility thatRH1951 and AK1603 in our study, and D.R. in thestudy of Scott et al., might show impaired recognitionof emotional prosody on some tasks, because of theirdamage to right hemisphere structures other than theamygdala. This possibility would be very consonantwith ®ndings that damage to right hemisphere [34±38,41,42], and to basal ganglia [44], perhaps especiallyto right basal ganglia [45], impairs recognition ofemotional prosody. Our interpretation is very consist-ent with that given in a study of another patient withbilateral amygdala damage, subject S.P. [23]. Like oursubject SM046, subject S.P. had no damage to basalganglia, and she was not impaired in recognizingemotional prosody.

Given our ®ndings, we must conclude that thehuman amygdala is not essential to recognize emotionin prosody. Nonetheless, the present results leave openthe possibility that the amygdala may normally beinvolved in emotional prosody recognition, eventhough not absolutely necessary, as indicated by recentresults from functional imaging [24]. Furthermore, wewish to stress that the present results pertain speci®-cally to recognizing emotion from human voice pro-sody; it remains possible that the amygdala will turnout to be critical for recognizing emotions in classes ofauditory stimuli other than prosody.

Acknowledgements

We thank Denise Krutzfeldt for scheduling subjects,and Jeremy Nath for help with testing. This study wassupported by a Sloan Research Fellowship and aFIRST award from NIMH to R.A., and by a programproject grant from the National Institute forNeurological Diseases and Stroke and a grant fromthe Mathers Foundation to Antonio R. Damasio.

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