Unseen-facial-and-bodily-expressions-trigger-fast-emotional-reactions_2009_Proceedings-of-the-National-Academy-of-Sciences-of-the-United-States-of-America.pdf

Unseen facial and bodily expressions trigger fast

emotional reactions

Marco Tamietto a,b,c,1 , Lorys Castelli b , Sergio Vighetti d , Paola Perozzo e , Giuliano Geminiani b , Lawrence Weiskrantz f,1 ,

and Beatrice de Gelder a,g,1

a Cognitive and Affective Neuroscience Laboratory, Tilburg University, P.O. Box 90153, 5000 LE Tilburg, The Netherlands; b Department of Psychology,

University of Torino, via Po 14, 10123 Torino, Italy; c Institute for Scientiﬁc Interchange (ISI) Foundation, Viale S. Severo 65, 10133 Torino, Italy; d Department

of Neuroscience, University of Torino, via Cherasco 15, 10126 Torino, Italy; e Centro Ricerche in Neuroscienze (Ce.R.Ne.), Fondazione Carlo Molo, via della

Rocca 24/bis, 10123 Torino, Italy; f Department of Experimental Psychology, University of Oxford, South Parks Road, Oxford OX1 3UD, United Kingdom;

and g Athinoula A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital, Harvard Medical School, Building 75, Room 2132-4,

Charlestown, MA 02129

Contributed by Lawrence Weiskrantz, August 21, 2009 (sent for review June 23, 2009)

The spontaneous tendency to synchronize our facial expressions

with those of others is often termed emotional contagion. It is

unclear, however, whether emotional contagion depends on visual

awareness of the eliciting stimulus and which processes underlie

the unfolding of expressive reactions in the observer. It has been

suggested either that emotional contagion is driven by motor

imitation (i.e., mimicry), or that it is one observable aspect of the

emotional state arising when we see the corresponding emotion in

others. Emotional contagion reactions to different classes of con-

sciously seen and ‘‘unseen’’ stimuli were compared by presenting

pictures of facial or bodily expressions either to the intact or blind

visual ﬁeld of two patients with unilateral destruction of the visual

cortex and ensuing phenomenal blindness. Facial reactions were

recorded using electromyography, and arousal responses were

measured with pupil dilatation. Passive exposure to unseen ex-

pressions evoked faster facial reactions and higher arousal com-

pared with seen stimuli, therefore indicating that emotional con-

tagion occurs also when the triggering stimulus cannot be

consciously perceived because of cortical blindness. Furthermore,

stimuli that are very different in their visual characteristics, such as

facial and bodily gestures, induced highly similar expressive re-

sponses. This shows that the patients did not simply imitate the

motor pattern observed in the stimuli, but resonated to their

affective meaning. Emotional contagion thus represents an in-

stance of truly affective reactions that may be mediated by visual

pathways of old evolutionary origin bypassing cortical vision while

still providing a cornerstone for emotion communication and affect

sharing.

shown in animal research (6). The clearest example is provided

by patients with lesions to the visual cortex, as they may reliably

discriminate the affective valence of facial expressions projected

to their clinically blind visual field by guessing (affective blind-

sight), despite having no conscious perception of the stimuli to

which they are responding (7, 8). But it is still unknown whether

nonconscious perception of emotions in cortically blind patients

may lead to spontaneous facial reactions or to other psychophysi-

ological changes typically associated to emotional responses. Fur-

thermore, whether emotional processing in the absence of cortical

vision is confined to specific stimulus categories (e.g., facial expres-

sions) or emotions (e.g., fear) is still the subject of debate (9).

One related issue regards the processes underlying emotional

contagion. A current proposal posits that observable (i.e., ex-

pressive) aspects of emotional contagion are based on mimicry

(1–3). According to this view, we react to the facial expression

seen in others with the same expression in our own face because

the perception of an action, either emotionally relevant or

neutral, prompts imitation in the observer; a process that implies

a direct motor matching between the effectors perceived and

those activated by the observer (motor resonance) (10). An

alternative account considers emotional contagion as an initial

marker of affective, instead of motor-mimetic, reactions that

unfold because the detection of an emotional expression induces

in the observer the corresponding emotional state (11, 12). Since

the same emotional state may be displayed by different expres-

sive actions such as facial gestures or body postures, there is no

need to postulate a direct motor matching between the observed

and executed action, providing the two convey the same affective

meaning (13, 14). Therefore, exposing participants to facial as

well as bodily expressions of the same emotion would contribute

toward the disentanglement of motor from affective accounts of

emotional contagion, because it enables one to assess whether

stimuli that are very different in their visual characteristics

nevertheless trigger similar affective and facial reactions in the

observer.

In the present study, we addressed these debated issues within

a single experimental design applied to two selected patients,

D.B. and G.Y., with unilateral destruction of occipital visual

cortex and ensuing phenomenal blindness over one half of their

visual fields. These patients provide a unique opportunity to

compare directly and under the most stringent testing conditions

emotional reactions to different classes of (consciously) seen and

affective blindsight

electromyography

emotional body language

motor resonance

emotional contagion

face

F acial and bodily gestures play a fundamental role in social

interactions, as shown by the spontaneous tendency to syn-

chronize our facial expressions with those of another person

during face-to-face situations, a phenomenon termed emotional

contagion (1). This rapid and unintentional transmission of

affects across individuals highlights the intimate correspondence

between perception of emotions and expressive motor reactions

originally envisaged by Darwin. Moreover, emotional contagion

has been proposed as the precursor of more complex social

abilities such as empathy or the understanding of others’ inten-

tions and feelings (2, 3). Ambiguity nevertheless persists about

the nature of emotional contagion, and the neuropsychological

mechanisms underlying automatic expressive reactions in the

observer are still underexplored.

A crucial question concerns the degree of automaticity of

emotional contagion and the role of visual awareness for the

eliciting stimulus in the unfolding of facial reactions. Available

evidence shows that perceptual mechanisms that bypass visual

cortex are sufficient for processing emotional signals, most

notably facial expressions (4, 5), akin to phenomena previously

Author contributions: M.T. and B.d.G. designed research; M.T., S.V., P.P., L.W., and B.d.G.

performed research; M.T., L.C., S.V., and G.G. analyzed data; and M.T., L.W., and B.d.G.

wrote the paper.

The authors declare no conﬂict of interest.

1 To whom correspondence may be addressed. E-mail: degelder@nmr.mgh.harvard.edu,

m.tamietto@uvt.nl, or larry.weiskrantz@psy.ox.ac.uk.

This article contains supporting information online at www.pnas.org/cgi/content/full/

0908994106/DCSupplemental .

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Fig. 1. EMG responses in patient D.B. ( A ) Mean responses in the ZM for seen stimuli. ( B ) Mean responses in the ZM for unseen stimuli. ( C ) Mean responses in

the CS for seen stimuli. ( D ) Mean responses in the CS for unseen stimuli. Frame color on the stimuli corresponds to coding of EMG response waveforms to the

same class of stimuli.

‘‘unseen’’ stimuli. In fact, all parameters of stimulus presentation

may be kept constant while simply varying the position where the

stimuli are projected (intact vs. blind visual field). Furthermore,

reactions arising in response to unseen stimuli in these subjects

can be unambiguously considered to be independent of early

visual cortical processing and also of conscious perception.

Facial and bodily expressions were presented in alternating

blocks either to the intact or to the blind visual field for2sin

a simple 2

EMG Results. Figs. 1 and 2 display the mean rectified EMG

responses from prestimulus baseline in patients D.B. and G.Y.,

respectively.

D.B. Amplitude Profile. Mean peaks of rectified EMG response

amplitudes were subjected to a 2 2 2 factorial design with

emotion (happiness vs. fear), expression (face vs. body), and

visual field (intact vs. blind) as within-subjects factors. A sepa-

rate repeated-measures analysis of variance (ANOVA) was

performed for each muscular region.

ZM activity was enhanced in response to happy as compared

to fearful expressions, as shown by the significant main effect of

emotion [F (1, 31) 644.2, P 0.0001]. No other main effect

or interaction resulted in significant outcomes [F (1, 31) 2.99,

P 0.093; for all factors and interactions]. This indicates that

facial and bodily expressions of happiness were equally effective

in inducing a spontaneous ZM response that, in turn, was similar

under conditions of either conscious or nonconscious stimulus

perception.

The CS was more activated by fearful than by happy expres-

sions [F (1, 31)

2 exposure paradigm. Within each block, fearful or

happy expressions were randomly intermingled. Facial move-

ments were objectively measured through electromyography

(EMG) to index expressive facial responses unknowingly gen-

erated by the patients. Specifically, activity in the zygomaticus

major (ZM) and corrugator supercilii (CS) muscles was re-

corded, as these twomuscles are differentially involved in smiling

or frowning, respectively (15). Pupil dilatation was also inde-

pendently assessed as a psychophysiological index of autonomic

activity that might be expected to accompany early stages of

emotional, but not motor-mimetic, responses (16). In fact, phasic

pupil dilatation provides a sensitive measure of increase in

autonomic arousal induced by sympathetic system activity (17).

Finally, when stimulus offset was signaled by an acoustic tone,

the patients were asked to categorize by button-press the emo-

tional expression just presented (happy or fearful) in a two-

alternative forced-choice (2AFC) task, thus providing a behav-

ioral measure of emotion recognition. In blocks when the stimuli

were projected to their blind field, the patients were required to

‘‘guess’’ the emotion displayed.

405.8, P

0.0001]. There was also a significant

emotion

expression

visual field interaction [F (1, 31)

4.29,

0.047]. Posthoc Bonferroni tests on the three-way interac-

tion showed that fearful facial expressions evoked greater CS

response than fearful bodily expressions, but only when the

stimuli were projected to the intact field and, therefore, con-

sciously perceived ( P 0.016). Conversely, facial and bodily

expressions of fear evoked the same CS activity when presented

to the blind field ( P 1).

Results

Behavioral Results. All expressions were correctly recognized

significantly above chance level by D.B. (mean accuracy in the

seeing field: 90.6%; in the blind field: 87.6%; P 0.0001, by

binomial tests for all eight conditions) and G.Y. (mean accuracy

in the seeing field: 86.8%; in the blind field: 73.5%; P

D.B. Temporal Profile. An ANOVA with the same factors and

levels considered previously was also computed on mean time of

peak amplitudes data to reveal possible differences in the time

unfolding of the EMG response.

In the ZM, the main effect of emotion and of visual field were

significant, as well as their interaction [F (1, 31)

0.05)

( Tables S1 and S2 ) . Noteworthy, accuracy of (nonconscious)

emotion discrimination in the blind field was not significantly

different from that in the seeing field and was not inf luenced by

either affective valence (happy vs. fear) or type of expression

(faces vs. bodies) [D.B.:

205.5, P

0.0001; F (1, 31)

0.0001;

respectively]. Posthoc comparisons on the interaction showed

that the EMG response to the happy expressions (i.e., to those

expressions that boosted ZM activity) was significantly faster

(peaking at around 900 ms from stimulus onset) when the stimuli

were presented to the blind field, as compared to the seeing field

(when peak activity occurred at around 1,200 ms) ( P 0.0001).

This effect was not present in response to fearful expressions that

93.1, P

0.0001; F (1, 31)

65.7, P

2 (1)

0.001, P 0.95, for all cross-tabulations]. This confirms previous

results of accurate discrimination of facial expressions in G.Y.

and extends the same findings to bodily expressions and to

patient D.B., who has the opposite field of cortical blindness.

2 (1) 0.001, P 0.99; G.Y.:

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Fig. 2. EMG responses in patient G.Y. ( A ) Mean responses in the ZM for seen stimuli. ( B ) Mean responses in the ZM for unseen stimuli. ( C ) Mean responses in

the CS for seen stimuli. ( D ) Mean responses in the CS for unseen stimuli. Frame color on the stimuli corresponds to coding of EMG response waveforms to the

same class of stimuli.

produced a similar temporal profile of the ZM activity in both

visual fields ( P 1).

A similar pattern of results was also observed in the CS muscle,

with a significant main effect of emotion, of visual field, and a

significant emotion visual field interaction [F (1, 31) 4041.9,

P 0.0001; F (1, 31) 78.9, P 0.0001; F (1, 31) 61.9, P

0.0001; respectively]. CS activity reached peak amplitude more

rapidly in response to nonconsciously than consciously perceived

fearful expressions (around 900 ms vs. 1,100 ms from exposure,

respectively) ( P 0.0001). Even in this case, the faster response

to unseen stimuli was specifically associated with the emotion

that evoked greater CS activity, as this effect was not observed

in response to happy expressions ( P 0.81).

response to unseen (peaking about 900 ms after stimulus expo-

sure) than seen fearful expressions (1,100 ms) ( P 0.0001).

Happy expressions, which failed to trigger CS activity, did not

induce a different temporal response as a function of conscious

or nonconscious stimulus perception ( P 1).

Pupillometric Results. Mean papillary response waveforms from

baseline are shown in Fig. 3 for D.B. and G.Y.

D.B. Amplitude Profile. Mean peak amplitudes of phasic pupil

dilatation were submitted to a repeated-measures ANOVA with

the same factors and levels previously considered in the analysis

of EMG data. There was a significant main effect of emotion,

showing that pupillary dilatation was boosted more by fearful

than happy expressions [F (1, 31)

55.2, P

0.0001]. The

G.Y. Amplitude Profile. The ZM was more reactive to happy than

to fearful expressions [F (1, 31) 25.8, P 0.0001]. The

expression

emotion

visual field interaction was also significant [F (1,

31)

0.03], as fearful, but not happy, expressions

evoked greater dilatation when presented to the blind as con-

trasted to seeing visual field ( P

5.2, P

visual field and the emotion

expression

visual field interactions also titled out significant [F (1, 31)

5.8, P 0.02; F (1, 31) 5.5, P 0.03; respectively]. Posthoc

testing revealed that happy faces induced grater ZM response

amplitude than happy bodies in the seeing visual field ( P

0.04), but elicited the same amplitude when shown in the blind

field ( P

0.013). Noteworthy, the effect

of expression or any interaction with this factor did not reach

significance, showing that facial and bodily expressions were

equally valid in inducing physiological arousal [F (1, 31)

1.1,

0.3].

1).

CS activity increased in response to fearful but not to happy

expressions, as shown by the significant main effect of emotion

[F (1, 31) 317.8, P 0.0001]. No other factor or interaction

resulted significant, thereby indicating similar CS responses to

faces and bodies alike, and no difference between the blind and

intact field [F (1, 31) 1.7, P 0.2].

D.B. Temporal Profile. The same ANOVA computed on amplitude

data was also performed on mean time of peak amplitudes,

showing no significant main effect or interaction [F (1, 31) 1.4,

P 0.2]. This indicates that the temporal profile of pupillary

dilatation was similar for all conditions, peaking in the time-

range 1,120–1,260 ms from stimulus onset.

G.Y. Temporal Profile. The ANOVA computed on the ZM showed

a significant effect of emotion, visual field, and of their inter-

action [F (1, 31)

G.Y. Amplitude Profile. The ANOVA showed a grater pupillary

dilatation in response to fearful expressions, as indicated by the

significant factor of emotion [F (1, 31) 52.2, P 0.0001].

Although the emotion visual field interaction only approached

statistical significance [F (1, 31) 3.5, P 0.07], the trend was

in the same direction reported for D.B., with higher dilatation

when fearful expressions were presented to the blind visual field.

0.0001;

F (1, 31) 9.3, P 0.005; respectively]. The interaction indicates

that happy expressions induced faster ZM activity when shown

to the blind field (peaking at around 1,000 ms from stimulus

onset) as contrasted to the intact field (peaking at around 1,300

ms) ( P

38.7, P

0.0001; F (1, 31)

43.7, P

0.0001); an effect that was not observed for fearful

expressions ( P 0.6).

The CS showed a temporal profile similar to that reported for

the ZM, with the factors emotion, visual field, and emotion

visual field resulting statistically significant [F (1, 31)

G.Y. Temporal Profile. Mean peak of pupillary dilatation took

place for all conditions around the time-range 1,120–1,280 ms

from stimulus onset. No main effect or interaction was found in

the ANOVA assessing the temporal profile of peak pupillary

dilatation [F (1, 31) 3.9, P 0.06, for all factors and

interactions].

2482.1,

P 0.0001; F (1, 31) 48.8, P 0.0001; F (1, 31) 18.3, P

0.0002; respectively]. Activity in the CS unfolded more rapidly in

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Fig. 3. Pupil responses in patients D.B and G.Y. ( A ) Mean pupil responses for seen stimuli in patient D.B. ( B ) Mean pupil responses for unseen stimuli in patient

D.B. ( C ) Mean pupil responses for seen stimuli in patient G.Y. ( D ) Mean pupil responses for unseen stimuli in patient G.Y. Frame color on the stimuli corresponds

to coding of pupil response waveforms to the same class of stimuli.

Discussion

Emotional Contagion for Seen and Unseen Inducers. The first note-

worthy finding is that passive exposure to either seen or unseen

expressions resulted in highly comparable psychophysiological

responses that systematically ref lected the affective valence and

arousal components of the stimuli. Specifically, happy expres-

sions selectively modulated EMG activity in the ZM, whereas

fearful expressions increased responses in the CS. Consistent

with expressive facial reactions, we also observed emotion-

specific pupil responses indicative of autonomic arousal, with

increased magnitude of pupillary dilatation for fearful as com-

pared to happy expressions. These pupillary changes cannot be

ascribed to physical parameters of the stimuli (e.g., brightness or

light f lux changes), because the different stimuli were matched

in their physical characteristics such as size and mean luminance.

Moreover, pupillary changes associated with these basic stimulus

attributes or with orienting responses have faster latencies than

those related to arousal responses (around 250 ms vs. 1,000 ms)

(17).

Autonomic activity is generally considered to ref lect the

intensity rather than the valence of the stimuli. Therefore, the

greater dilatation in response to fearful than to happy stimuli

may simply indicate that the former stimuli were more effective

than the latter in inducing an arousal response. An alternative

explanation would be that coping with threatening situations

requires greater energy resources to the organism. There is

indeed some evidence that several basic emotions, such as

happiness, fear or anger, are associated with specific patterns of

autonomic nervous system activity (18). Nevertheless, the pos-

sibility to differentiate between emotions on the base of their

specific autonomic architecture would require simultaneous

recording of various measures (e.g., pupil size, heart rate, skin

conductance, and blood pressure) and thus remains speculative

as far as the present study is concerned.

Previous evidence of spontaneous expressive reactions to

nonconsciously perceived emotional stimuli is based only on one

study by Dimberg and colleagues that recorded facial EMG to

backwardly masked, and thus undetected, facial expressions (19).

However, unlike in the present case, these responses were not

contrasted to those generated by conscious stimulus perception,

therefore preventing a direct comparison of the conscious vs.

nonconscious processing modes. Moreover, experimentally in-

duced nonconscious vision in neurologically intact observers is

liable to intersubject variability and to the different criteria to

assess below-awareness thresholds (20, 21). Hence, masking

constitutes a weaker case in support of emotional contagion for

unseen stimuli compared to the study of patients with permanent

cortical blindness.

Aside from their similarities, we also found that emotional

contagion responses have different amplitude and temporal

dynamics, depending on whether the eliciting stimulus is seen or

unseen. Indeed, facial reactions were faster and autonomic

arousal was higher for unseen than seen stimuli. This effect was

not an unspecific one (e.g., a generalized speeding up of facial

reactions in both muscles irrespectively of the stimulus valence),

but was selective for the emotion displayed by the stimuli, arising

for the ZM in response to happy expressions and for the CS in

response to fearful expressions. Likewise, enhanced pupillary

dilatation for unseen as compared to seen stimuli was specific to

fearful expressions.

Evidence that affective reactions unfold even more rapidly

and intensely when induced by a stimulus of which the subject is

not aware is in line with data showing that emotional responses

may be stronger when triggered by causes that remain inacces-

sible to introspection (22). These temporal diversities are also

consistent with the neurophysiological properties of partly dif-

ferent pathways thought to sustain conscious vs. nonconscious

emotional processing. Indeed, conscious emotional evaluation

involves detailed perceptual analysis in cortical visual areas

before the information is relayed to emotion-sensitive structures

such as the amygdala or the orbitofrontal cortex (6). On the

other hand, nonconscious emotional processing is carried out by

a subcortical route that rapidly conveys coarse information to the

amygdala via the superior colliculus and pulvinar, thereby

bypassing primary sensory cortices (4, 5, 23).

The Nature of Emotional Contagion. To what extent do emotional

contagion responses originate from motor mimicry or rather are

induced by an emotional state in the observer contingent upon

visual detection of the stimulus valence? The present results

plead in favor of the second alternative for the following reasons.

First, facial and bodily expressions evoked very similar facial

reactions in the observers. This convincingly demonstrates that

the patients did not simply match the muscular pattern observed

in the stimuli, but rather resonated to their affective meaning

with relative independence from the information-carrier format.

According to the direct motor-matching hypothesis (2), we

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should have detected no facial reactions in response to bodily

expressions, because no simple or direct motor correspondence

exists between facial muscles responsible for engendering an

expressive reaction in the observer’s face, on the one hand, and

arm/trunk muscles that convey emotional information in the

projected body postures, on the other. Admittedly, it is possible

that facial reactions arise in response to bodily expressions

because of a filling-in process that adds to the body stimulus the

missing facial information. Nevertheless, this possibility would

not provide an argument in favor of the motor account of

emotional contagion, because it would indicate that an observed

expressive action is simulated only after its meaning has been

previously evaluated.

Second, unseen face and body stimuli triggered emotion-

specific expressive responses. As discussed above, these highly

automatic reactions fit well with current evidence that phyloge-

netically ancient structures are able to attribute emotional value

to environmental stimuli and to initiate appropriate responses

toward them even in the absence of stimulus awareness and

visual input from the cortex (4, 6). Although mimicry of non-

emotional expressions may also unfold spontaneously, as in the

case of contagious yawning or orofacial imitation of adult facial

gestures in newborn infants, these phenomena typically occur

under conditions of normal visibility of the eliciting stimuli (24,

25). Therefore, motor resonance seems to exhibit a lesser degree

of automaticity than emotional processing, as it is liable to

attentional load and visual awareness (26). Since perceptual

consciousness of the stimulus was prevented in our patients by

damage to the visual cortex, motor resonance is unlikely to

explain emotional contagion responses, at least for stimuli

projected to the cortically blind field.

Lastly, in addition to expressive facial reactions, we have been

able to show arousal responses induced by the presentation of

faces and bodies alike. This physiological component is a typical

marker of ongoing emotional responses and was found to covary

with the affective valence of the stimuli, being higher for fearful

than for happy expressions (16, 18). A comparison of the

temporal profiles of facial and pupillary reactions reveals that

the two parameters have a closely similar unfolding over time,

both peaking at around 1,100 ms from stimulus exposure. This

temporal coincidence between expressive motor reactions and

arousal responses is consistent with the notion that detection of

emotional signals activates affect programs of old evolutionary

origin that encompass integrated and simultaneous outputs like

expressive behaviors, action tendencies, and autonomic changes

(13, 27). The processing sequence envisaged by motor theories

of emotional contagion, on the other hand, predicts an initial

nonemotional mimicry, possibly carried out by the cortical

mirror-neurons system, and a subsequent emotional response

when the information is transferred via the insula to subcortical

limbic areas processing its emotional significance (2). Even

though our data were acquired with a temporal resolution of the

order of milliseconds, there was no indication of such sequencing

between facial and pupillary responses in the patients.

Of course, even though our findings show that emotional

contagion represents an instance of truly affective reactions in

the observer that is not reducible to, nor dependent on, motor

resonance, they do not rule out the possible involvement of

nonaffective imitative components. For instance, motor reso-

nance responses may take place at later stages and under specific

contextual conditions to modulate emotional contagion (28).

There is evidence in the present data that this might be the case.

Indeed, facial reactions were found to be more intense in

response to the facial than bodily expressions, but notably under

conditions of conscious stimulus perception only. Importantly,

however, expressive responses were faster for nonconscious

stimuli and in the latter case no difference between faces and

bodies was found. This suggests that motor resonance may

facilitate emotional contagion responses, but critically depends

on perceptual awareness and cortical vision and comes into play

only after nonconscious perceptual structures that bypass visual

cortex have evaluated the affective valence of the stimuli.

Emotion Recognition, Affective Blindsight, and Conscious Experience.

A longstanding issue in affective blindsight is what stimulus

categories or attributes can be processed in the absence of

cortical vision and awareness to enable emotion recognition

(29). The initial reports used facial expressions and affective

pictures, with positive results for the former stimuli and negative

results for the latter, therefore suggesting a special status for

faces in conveying nonconscious emotional information (7–9).

The present results show that affective blindsight arises also for

bodily expressions, consistent with our previous findings that the

same body stimuli may be processed implicitly in patients with

hemispatial neglect (30). D.B. and G.Y. were in fact both able to

discriminate correctly the emotional valence of unseen facial as

well as bodily expressions in a 2AFC task. Overall, the findings

indicate that nonconscious recognition of emotions in blindsight

is not specific for faces, but rather for biologically primitive

expressions at relatively low special frequencies.

To what extent is affective blindsight really affective? In

principle, nonconscious discrimination of emotional expressions

may not be different from discrimination of complex neutral

images of animals or objects (31). The phenomenon might thus

be confined to the visual domain and reduced to a specific

instance of shape recognition. The present findings, however,

provide direct evidence that this is not the case. Notwithstanding

the patients had no conscious experience of the stimuli presented

to their blind field, they were actually in an emotional state, as

shown by the presence of expressive and arousal responses

typical of emotions. The presence of somatic changes that go

beyond activity in the visual system is relevant to understand

what might be the process that leads blindsight patients to guess

correctly the emotion of stimuli they do not see. It is possible the

patients unwittingly ‘‘sense’’ the somatic changes elicited by the

stimulus and use it as a guide to orient the decision about what

emotion is displayed. This surmise is reminiscent of the facial-

feedback hypothesis (32) or of more elaborated theories about

the relationship between bodily changes and emotion under-

standing, such as the somatic-marker hypothesis (33). It is also

consistent with previous reports showing that patients with

visual agnosia, thereby unable to discriminate consciously be-

tween different line orientations or shapes, may nevertheless use

kinesthetic information from bodily actions to compensate for

their visuoperceptive deficits (34). This issue clearly deserves

further study, and attention needs to be paid in the future to the

affective resonance and inf luence exerted by unseen emotions

over conscious experience and intentional behavior toward the

normally perceived world.

Materials and Methods

Subjects. D.B. is a 69-year-old male patient who underwent surgical removal

of his right medial occipital lobe at age 33 because of an arterious venus

malformation, giving raise to a left homonymous hemianopia that 44 months

postoperatively contracted to a left inferior quadrantanopia (35).

G.Y. is a 53-year-old male patient with right homonymous hemianopia

following damage to his left medial occipital lobe at age 7 due to a traumatic

brain injury; see ref. 36 for a recent structural and functional description of

G.Y.’s lesion and outcomes.

Both patients gave informed consent to participate in the study.

Stimuli and Procedure. Face stimuli were modiﬁed from Ekman’s series (37),

and body stimuli were modiﬁed from the set developed by de Gelder et al.

(11). As in the original set of stimuli, facial information was removed from

body images by blurring. The whole set used in the present study consisted of

32 gray-scale images (16 faces, half of which expressing happiness and half

fear, and 16whole-body postures, half expressing happiness and half fear). All

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