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1National Institute of Neuroscience, National Center of Neurology and Psychiatry, Tokyo; 2Collaboration of Regional Entities on Science and Technology, Japan Science and Technology Agency, Saitama; and 3Primate Research Institute, Kyoto University, Aichi, Japan
Submitted 3 May 2006; accepted in final form 13 December 2006
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSREFERENCES |
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSREFERENCES |
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; Ekman 1969). For example, seeing an angry face and hearing an angry voice lead to the perception of a person's anger and then the generation of appropriate responses to that emotion. The amygdala has been implicated in the evaluation of emotional meaning (Rolls 2000) and damage to the amygdala results in abnormalities in the generation of primate emotional behavior (Klüver and Bucy 1938, 1939; Meunier et al. 1999). The responsiveness of the amygdala to facial emotion has been well studied. Neurons in the monkey amygdala are sensitive to facial emotion (Kuraoka and Nakamura 2006; Leonard et al. 1985; Nakamura et al. 1992). Previous functional neuroimaging and neuropsychological studies demonstrated the activation of the amygdala during the recognition of facial emotion in humans (Adolphs et al. 1994; Breiter et al. 1996; Morris et al. 1996; Young et al. 1995).
However, the responsiveness of neurons to vocal emotion and the relationship between responsiveness to facial emotion and that to vocal emotion are still unclear. The amygdala receives extensive inputs from not only higher-order visual areas such as the inferotemporal cortex, but also higher-order auditory areas such as the superior temporal gyrus (Amaral et al. 1992; Turner et al. 1980). Therefore the amygdala is one of the most plausible candidates for the brain region processing signals for facial and vocal emotions. Scott et al. (1997) reported the case of a patient with a damaged amygdala who suffered from an impaired recognition of vocal emotion as well as facial emotion.
In this study, to examine neuronal mechanisms underlying the generation of appropriate responses to facial and vocal emotions, we recorded the activity of single neurons in the monkey amygdala in response to species-specific emotional expressions and examined the responsiveness of neurons to facial and vocal emotions.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSREFERENCES |
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Three female rhesus monkeys (Macaca mulatta, 5.6–6.8 kg, 5–9 yr old) were used as subjects. Although each of these monkeys was housed in an individual cage, the animals had normally experienced facial and vocal communications with others. They could see other individuals and hear their voices, but could not make body contact with each other. Water was withheld before each daily session and juice was given as a reward in an experimental room. Supplemental water and vegetables were given after the session when needed. Food (monkey chow) was available without restriction. Neuronal activity was recorded from four hemispheres of three monkeys. All experiments were carried out in accordance with the guidelines outlined in the Guide for the Care and Use of Laboratory Animals of the National Research Council (1996) and the Guide for Care and Use of Laboratory Primates published by the Primate Research Institute, Kyoto University (1986, 2002).
Task procedure
All experiments were performed in a dark soundproof room. The monkeys were trained to perform a fixation task (Fig. 1). A monkey sat in a primate chair and faced a 21-in. multiscan monitor (GDM-F520; Sony, Tokyo, Japan) placed 30 cm from the monkey's eyes. When the monkey pressed a lever, a yellow fixation spot appeared at the center of a colored monitor placed 30 cm in front of the eyes. After the monkey kept the lever pressed and fixated on the spot for 1,000 ms, a test stimulus was presented for 1,000 ms; thereafter, the yellow spot was replaced by a red spot after a certain period (300–1,500 ms). If the monkey released the lever within 800 ms of spot replacement, the monkey was rewarded (Fig. 1). The eye position was continuously monitored using a charge-coupled device (CCD) camera system. If the monkey's eye deviated more than 1.5° from the fixation spot or if the monkey released the lever during a trial, the trial was terminated without providing any reward.
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Original test stimuli were 1,000-ms full-color video clips with sounds, presented on a gray background (30 x 20°). The sound was presented through a speaker on the monitor at about 70 dB SPL measured at the level of the monkey's ear. We prepared nine monkey-specific emotional expressions (three models, monkeys A, B, and C, showing three emotional expressions). The three emotional expressions were aggressive threat, coo, and scream. An aggressive threat is often expressed by a dominant individual motivated by the tendency to attack. The eyes are staring wide open at the opponent with the eyelids fully apart. The mouth corners are brought forward and the lips are fully tensed. The vocalizations of this expression are low-pitched grunts. A coo has multiple meanings. This is often expressed in response to food presented and by monkeys separated from their group members or mothers. This is a response expressing the need for body comfort or the opportunity to feed. The mouth is slightly open and the mouth corners are pulled forward. The vocalization is a clear, moderately pitched "ooo." A scream is often expressed by a subordinate attacked or threatened by a dominant individual. The eyes are wide open and the ears are folded back. The mouth is open and the mouth corners and lips are completely retracted, resulting in completely bared teeth. The vocalizations of this expression are often prolonged high-pitched screams. We also used two human stimuli and two object stimuli. The monkeys had seen and heard the face and voice of the persons they had encountered in their everyday life. Thus we considered that these human stimuli had some but species-specific behavioral importance for the monkeys. In contrast, the monkeys had neither seen nor heard the images and sounds of the objects before this experiment. Thus the monkeys acquired the knowledge of the association between the image and sound of the objects during the experiment. In total, 13 stimuli were used in this study. After completing the task with the combined facial and vocal stimuli, the activity of neurons was recorded while a visual (face) or an auditory (voice) element of a monkey-specific emotional expression was presented alone to determine the element crucial to a neuronal response.
Surgery
After the monkeys had learned the fixation task, a head-holding device and a recording cylinder were implanted on the skull. Surgery was carried out under pentobarbital sodium anesthesia [20–25 mg/kg body weight, administered intravenously (iv)]. Antibiotics were administered postoperatively for >1 wk to prevent infection. After a recovery period of >10 days, each monkey was retrained, for them to become accustomed to the head restraint, and recordings were started.
Recording procedure
The action potentials of single neurons were recorded extracellularly from the amygdala of four hemispheres of three monkeys with a polyurethane-coated tungsten microelectrode (1.5–3.0 M
, 0.3 mm in diameter). The tungsten microelectrode was inserted through a guide tube (1.1 mm in diameter) fixed to a grid deep into the brain without distortion. A stainless steel guide tube was inserted through the dura to a depth of about 5 mm above the amygdala, estimated from magnetic resonance (MR) images. The electrode was advanced using a hydraulic microdrive (Narishige, Tokyo, Japan), while neuronal activity was monitored.
The action potentials were discriminated and converted into pulses using a window discriminator (BAK Electronics, Germantown, MD). The timings of spikes of a single neuron and task events were stored on a PC with a time resolution of 0.5 ms. When the activity of a single neuron was isolated, a recording session was started. We presented all 13 stimuli under three conditions: audiovisual, visual, and auditory conditions. Under the audiovisual and visual conditions a full-color video picture was presented at the center of the monitor with a gray square (30 x 20°) as the background. Under the audiovisual and auditory conditions a sound was played through a speaker on the monitor at about 70 dB SPL measured at the level of the monkey's ears. If the neuronal activity remained isolated when the audiovisual condition had finished, the next condition was started. The second condition was either the visual condition or auditory condition and the third was the remaining condition. Under each condition, we presented the 13 stimuli pseudorandomly until each had appeared 10 times. Thus a recording session was composed of 130 trials.
Histological analysis
The locations of recorded neurons in the three monkeys were histologically identified on a series of coronal sections of the brain. Several microlesions were made in advance in the amygdala by passing an anodal current (3–4 µA, 600 µC) through Elgiloy microelectrodes. After completing all of the recording sessions, each monkey was deeply anesthetized with pentobarbital sodium (30–35 mg/kg body weight, iv) and the brain was perfused with saline and 10% buffered formalin. Ferrocyanide (2%) was mixed with the formalin solution to stain iron deposits from the Elgiloy electrodes by the Prussian blue reaction. The brains were frozen, sectioned coronally at 100-µm intervals, and stained with cresyl violet. The locations of neurons were determined using the sites of the microlesions as reference points. All boundaries were determined on the basis of previous studies (Amaral et al. 1992).
Data analysis
We reported properties of the visual responses of the amygdala neurons in our previous study (Kuraoka and Nakamura 2006). Here, we focused on different aspects of response properties of the amygdala neurons: multisensory responsiveness.
The stored data were analyzed off-line to determine whether the recorded neurons responded to any of the stimuli. Average peristimulus time histograms (bin width, 50 ms) and raster displays (bin width, 2 ms) for the 13 stimuli were constructed for each neuron. If the number of spikes of a neuron during the period from 100 to 1,100 ms after the onset of a stimulus was significantly different from that during a 1,000-ms control period immediately before the stimulus onset (Wilcoxon signed-ranks test, P < 0.01), the neuron was regarded as responsive to the stimulus.
To elucidate the effects of facial and vocal emotions on the responses of amygdala neurons, we carried out the following analyses. First, we examined whether the responses of the amygdala neurons to the visual stimuli were modulated when the auditory stimuli were combined. For the response of each neuron to the optimal monkey stimulus under the audiovisual condition, we used a well-established multisensory modulation index (Barraclough et al. 2005; Bell et al. 2003; Ghazanfar et al. 2005) to calculate the magnitude of the modulation using the following formula: multisensory modulation index (%) = 100 x [(AV – V)/V], where V represents mean responses of the neuron to the visual stimuli and AV represents those to the audiovisual stimuli. We also compared the response to the audiovisual stimuli with that to the visual stimuli using the Mann–Whitney U test. Next, if a neuron showed responses not only to the visual stimuli but also to the auditory stimuli, we examined the similarity of the neuronal responses to the monkey stimuli among the three stimulus conditions. We determined the correlation of the neuronal responses among the three stimulus conditions using the Friedman test.
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RESULTS |
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Optimal stimulus
For the 116 monkey-responsive neurons, we examined the optimal stimulus, which elicited maximal neuronal firing, for each amygdala neuron among the nine monkey-specific emotional expressions. As shown in Fig. 2, about one half of the monkey-responsive neurons (57/116, 49%) showed the maximal response to the scream (purple), 30% (35/116) showed the maximal response to the coo (blue), and the remaining 21% (24/116) showed the maximal response to the aggressive threat (yellow). Thus about one half of the monkey-responsive neurons preferred the scream to other types of emotion (chi-square test, P < 0.001). On the other hand, monkeys A, B, and C elicited the maximal responses of 31% (36), 41% (47), and 28% (33) of the 116 monkey-responsive neurons, respectively. There was no significant tendency that the emotional expressions of a certain monkey model frequently elicited the maximal responses from the amygdala neurons (chi-square test, P = 0.245). Taken together, the amygdala neurons preferred the scream to other types of emotion irrespective of the identity of the monkey model.
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To determine the element crucial to neuronal responses, the activity of the neurons was recorded while the visual (face) or auditory (voice) element of a monkey-specific emotional expression was presented alone. We successfully examined the activity of 79 monkey-responsive neurons under the audiovisual, auditory, and visual conditions.
Figure 3 shows the responses of a neuron recorded under the three conditions. This neuron showed the strongest response to the scream of monkey C and a weak response to the scream of monkey B, but a faint or no response to other monkey-specific emotional expressions under the audiovisual condition (Fig. 3A). When only the visual element of each stimulus was presented (visual condition, Fig. 3B), the same monkey-responsive neuron maintained its strong response to the same scream of monkey C and its weak response to the scream of monkey B. The overall pattern of responses under the visual condition was very similar to that under the audiovisual condition. However, when only the auditory element was presented (the auditory condition, Fig. 3C), this neuron showed no responses to any stimuli. The mean discharge rates of this neuron in response to the scream of monkey C under the audiovisual, visual, and auditory conditions were 13.3, 20.5, and 1.2 spikes/s, respectively, whereas the control rate was 2.7 spikes/s.
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Because many amygdala neurons (77 of 79 recorded under three stimulus conditions) responded to the visual stimuli, we examined the effect of auditory stimuli on the responses of the neurons to visual stimuli in 77 visual-stimuli–responsive amygdala neurons according to a previous study (Barraclough et al. 2005) and compared between their and our results. We calculated the multisensory modulation index (see METHODS). For a population, the multisensory modulation index was significantly >0 (Wilcoxon signed-ranks test, P < 0.05, Fig. 4). The mean magnitude and the SD of increase in the activity of the 77 neurons were 56.7 and 180%, respectively. Moreover, 39 neurons (39/77, 51%) showed a significantly larger magnitude of the response to the audiovisual stimuli than to the visual stimuli (Mann–Whitney U test, P < 0.05). In contrast, there were no neurons that showed a significantly smaller magnitude of the response to the audiovisual stimuli than to the visual stimuli. Thus the visual responses of the amygdala neurons were augmented by the simultaneous presentation of the auditory stimuli.
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Figure 5 shows the responses of a neuron that responded to facial and vocal emotions. This neuron showed the strongest response to the scream of monkey B under the audiovisual condition. This neuron showed the second and third strongest responses to the scream and aggressive threat of monkey A, respectively. No other stimuli elicited significantly strong responses from this neuron. Under the visual condition (Fig. 5B), the same neuron similarly showed the strongest response to the scream of monkey B and the second and third strongest responses to the scream and aggressive threat of monkey A. Even when only the auditory (voice) element of each stimulus was presented (the auditory condition, Fig. 5C), this neuron responded likewise. The sound of the scream of monkey B elicited the strongest response of the same neuron under the auditory condition. Furthermore, the sounds of the scream and aggressive threat of monkey A respectively elicited the second and third strongest responses from this neuron. The mean discharge rates of this neuron in response to the optimal stimulus under the audiovisual, visual, and auditory conditions were 22.1, 18.2 and 9.9 spikes/s, respectively, whereas the control rate was 0.2 spikes/s.
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We also examined the similarity of the stimulus-preference profiles of the other 15 neurons exhibiting significant responses to facial and vocal emotions. In 88% of the neurons (14/16), changes in discharge rate were significantly correlated among the three stimulus conditions (filled areas in Fig. 6, Friedman test, P < 0.05). Furthermore, in 75% of the neurons (12/16), the optimal stimulus was identical among the three stimulus conditions. These results demonstrate that most of the neurons responding to facial and vocal emotions maintained their stimulus-preference profiles even when the visual (face) or auditory (voice) element was removed: that is, these neurons showed "supramodal" responses to monkey-specific emotional expressions.
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We examined the locations of the monkey-responsive neurons within the amygdala. As shown in Fig. 8, we recorded the activity of the monkey-responsive neurons from various subnuclei of the amygdala, including the lateral, basal, accessory basal, medial, and central nuclei. Neurons predominantly conveying information about changes in facial configuration were distributed in all the nuclei examined in the amygdala (red dots in Fig. 8B; Table 1). However, neurons exhibiting the supramodal responses were concentrated in the central nucleus (yellow dots in Fig. 8B; Table 1). This biased distribution was statistically significant (chi-square test, P < 0.01)
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSREFERENCES |
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Effective stimuli for eliciting amygdala response
Previous studies (Leonard et al. 1985; Nakamura et al. 1992) examined the responsiveness of amygdala neurons to facial emotions. In the task of the study by Nakamura et al. not facial stimuli themselves but correct behavioral responses signaled rewards. In the task of the study by Leonard et al. not facial stimuli themselves but a circle or a square simultaneously presented with facial stimuli signaled rewards or punishments. Generally, it is difficult to activate amygdala neurons in such tasks. For example, only 35% of neurons examined were activated by visual stimuli such as monkey faces, human faces, foods, or nonfood objects in the study by Nakamura et al., whereas Leonard et al. reported that only 12% of amygdala neurons responded to visual stimuli, even though they used photographs of not only faces but also real faces. On the other hand, about one half (51%) of the amygdala neurons examined in our study responded to at least one of the nine monkey-specific facial expressions. The difference in the proportion of responsive neurons between our present study (116/227) and the study by Nakamura et al. (144/408) or Leonard et al. (there was no detailed description of the number of neurons, but 40 of 1,000 visual neurons at most responded primarily to facial stimuli) was statistically significant (chi-square test, P < 0.01 and P < 0.01, respectively).
The amygdala neurons were previously indicated to show good responsiveness to visual stimuli directly associated with reward or punishment. Sugase-Miyamoto and Richmond (2005) found that more than one half of basolateral amygdala neurons showed the responses to the visual stimuli that indicated how many trials remained to be completed before a reward. Paton et al. (2006) found that one half of amygdala neurons can dynamically change their responses to visual stimuli depending on association with rewards or punishments. However, our present study showed that visual stimuli not directly associated with rewards or punishments elicit good responses of the amygdala neurons. In our study, all stimuli were randomly presented and the same reward was provided to the monkeys irrespective of the stimulus presented. Therefore the difference in the proportion of responsive neurons among the studies did not arise from the reward-predicting activity found in the studies of Sugase-Miyamoto and Richmond (2005) and Paton et al. (2006).
We believe that motion pictures would be so effective in activating amygdala neurons that about one half of the neurons examined responded to the stimuli. We used movie clips as stimuli because dynamic changes in facial configuration are very important as signals of emotional expression. In humans, it was shown that representations of facial expressions of emotion contain information about dynamic and static properties (Kamachi et al. 2001). Human subjects can classify some emotional expressions, such as surprise, just by movements of certain points on the face (Bassili 1978). Normally, monkeys never see static pictures. Thus it is conceivable that the movie stimuli used in this study activated more amygdala neurons than the static images used in the cited previous studies.
Moreover, because monkey vocalizations as well as facial expressions are used to express their emotion, the vocal element of our stimuli might have also contributed to eliciting neuronal responses from the amygdala. Nishijo et al. (1988) also presented auditory and visual stimuli to monkeys and reported the responsiveness of monkey amygdala neurons to auditory stimuli. In our study, in about a one half of the neurons (51%, 39/77), the responses to the visual stimuli were augmented by the simultaneous presentation of the auditory stimuli. Because multisensory signals can facilitate communication (Partan and Marler 1999), we consider that the vocal and visual elements of our stimuli effectively activated amygdala neurons. Altogether, our results suggest that dynamic facial expressions with corresponding vocalizations in our study were effective in activating amygdala neurons.
Strong response to fear
Many previous studies (Adolphs et al. 1994; Breiter et al. 1996; Dolan et al. 2001; Morris et al. 1996; Phillips et al. 1998; Scott et al. 1997; Young et al. 1995) found the relationship between the human amygdala and fearful expression. A recent study showed normal discrimination of fearful faces of a patient with bilateral amygdala damage after instruction to look at the eyes (Adolphs et al. 2005). However, the patient was required only to discriminate fearful from happy faces, indicating that the ability of the patient to discriminate fearful from happy faces was intact. However, whether the ability of the patient to recognize fearful emotion was intact is unclear. Reportedly, the human amygdala is involved in recognizing not only fearful faces but also fearful voices (Dolan et al. 2001; Phillips et al. 1998; Scott et al. 1997) or fearful body expressions (Hadjikhani and de Gelder 2003). Thus it appears that the human amygdala plays a major role in recognizing fearful emotion regardless of sensory channels. Moreover, from the observation that the human amygdala showed stronger responses to fearful expression than to angry expression, it is considered to be involved in processing ambiguity of the source of threat (Whalen et al. 2001). Our results are consistent with this observation. Many neurons in the amygdala preferred the scream to the coo and aggressive threat. The scream is an emotional expression exhibited with strong fear by a subordinate threatened aggressively by a dominant individual (Gouzoules et al. 1984; Hinde and Rowell 1962; Van Hooff 1962). Thus these amygdala neurons are more sensitive to fearful expression that provides information to observers about the presence of threat, which is essential for animals to survive. Our data suggest the presence of a fear-detecting system in the monkey amygdala, similar to the human amygdala.
Because our monkey subjects had seen the stimuli many times, overt emotional reactions to the monkey-specific emotional expressions were not observed during recording sessions. However, the first several presentations of the monkey-specific emotional expression elicited strong overt emotional reactions, such as scream, grunt, lip smacking, and shaking the apparatuses. Therefore the scream repeatedly presented may have elicited covert emotional reactions in our monkey subjects even after overt emotional reactions had disappeared. However, further experiments—such as one that tests whether other emotional stimuli that elicit a similar emotional response result in similar neuronal activity of the monkey amygdale—are necessary.
Dominance of visual processing
When the activity of neurons in the amygdala was recorded while the visual (face) or auditory (voice) element of the monkey-specific emotional expression was presented alone, about three fourths of the monkey-responsive neurons (61/79, 77%) showed a strong response to the visual element but not to the auditory element, whereas only one amygdala neuron responded to just the auditory element alone. Therefore most monkey-responsive neurons examined seemed to predominantly convey information about changes in facial configuration. Several possibilities could explain the predominance of visual processing. The first is the priority of the visual system over other sensory modalities in nonhuman primates (Redican 1975). Rhesus monkeys use vocal signals in social interaction only 5% of the time (Altmann 1967). Thus amygdala neuronal activity reflects the dominant visual characteristics of monkey behavior. The second is the task procedure. In this study, the monkeys were required to fixate on the central spot of the display, thereby focusing their attention on visual cues. This could affect neuronal responsiveness in the amygdala. Another possibility is sampling bias because we inserted the electrodes vertically. The dorsal portion of the lateral nucleus of the amygdala receives inputs from visual areas, whereas its ventral portion receives inputs from auditory areas (Amaral et al. 1992); however, as shown in Fig. 8, the monkey-responsive neurons were distributed from the dorsal to the ventral portions of the amygdala. We consider the last possibility unlikely.
Audiovisual modulation in amygdala neurons
Several monkey studies showed audiovisual activity in response to biologically relevant stimuli in other brain areas such as the superior temporal sulcus (STS; Barraclough et al. 2005), the ventrolateral prefrontal cortex (VLPFC; Sugihara et al. 2006), and the auditory cortex (Ghazanfar et al. 2005). Barraclough et al. and Sugihara et al. found that 23% of STS neurons and 39% of VLPFC neurons showed neuronal activity modulation, respectively, and Ghazanfar et al. found that the local field potential (LFP) is modulated in 88% of the core region and 72% of the lateral belt region of the auditory cortex. In all three studies, the neural activity modulations were characterized by both enhancement and suppression. We also found that 51% of the amygdala neurons showed modulated activity when the audiovisual stimuli were presented compared with when the visual stimuli were presented. Because the amygdala has a strong connection with the STS (Amaral et al. 1992), the amygdala might receive multisensory inputs from the STS. Unlike the neuronal activity modulation observed by Barraclough et al., Sugihara et al., and Ghazanfar et al., however, that observed in the amygdala in our study was always characterized by enhancement. In addition, the proportion of neurons that showed enhanced responses to the audiovisual stimuli in the amygdala in our study was significantly larger than that in the STS in the study by Barraclough et al. or in the VLPFC in the study by Sugihara et al. (14/95 in the STS, 40/387 in the VLPFC, and 39/77 in the amydala, chi-square test, P < 0.01, in both comparisons). This is also true when we compared only the neurons in the lateral nucleus of the amygdala, which is the nucleus connected with the STS, with the neurons recorded in the STS by Barraclough et al. (14/95 in their study and 9/21 in our study, chi-square test, P < 0.01). Thus the visual response of amygdala neurons to facial emotion is generally enhanced by the simultaneous presentation of vocal emotion. Such enhancement of the visual response by vocal emotion would enable the monkey to reliably detect emotional signals and quickly generate an appropriate reaction.
However, there is another negative possibility. In our study, the monkeys saw the audiovisual stimuli more frequently than either a face or voice stimulus alone because we presented the audiovisual stimuli during searching and recording of the activity of neurons and either the visual or auditory stimuli during recording only. In contrast, the combined audiovisual stimuli were presented after the neurons had shown the responses to either a visual or auditory stimulus alone in the studies by Barraclough et al. and Ghazanfar et al. and both the audiovisual and the unimodal stimuli were presented during searching of the activity of neurons in the studies by Sugihara et al. Thus there is a possibility that the difference in results between our study and the other studies is explained by the stimulus presentation procedure. Moreover, it is also possible that we underestimated the effects of audiovisual modulation in the monkey amygdala because visual fixation suppresses multisensory effects in the superior colliculus (Bell et al. 2003). In our study, strict fixation (within 1.5° from the fixation spot) was required of the monkeys during the stimulus presentation periods. Although the details of the requirement in the study by Sugihara et al. were unknown, the requirement of our study was stricter than that in the other two studies (Barraclough et al. allowed monkeys to deviate their eyes from the fixation spot by 3.0° and monkeys in the study of Ghazanfar et al. were allowed eye movements within a video frame). Thus a strict fixation (i.e., greater attention on the fixation spot) might attenuate the effects of audiovisual modulation in the neurons of the primate amygdala and obscure the suppressed neuronal responses in the amygdala.
Supramodal representation of emotion
Unlike in the two previous studies examining the neuronal activity in the temporal lobe (Barraclough et al. 2005; Ghazanfar et al. 2005), here we found amygdala neurons responding to the visual and auditory elements of the monkey-specific emotional expressions. There is evidence that nonhuman primates, similar to humans, can detect the correspondence of visual information with auditory information during emotional communication (Evans et al. 2005; Ghazanfar and Logothetis 2003; Izumi and Kojima 2004). The modality-invariant or "supramodal" representation of emotion is suitable for the perception and production of the entire range of facial and vocal emotional behavior, constituting an essential part of communicative competence (Partan and Marler 1999; Rowe 1999), on which complex social interactions in human and nonhuman primates are based. In this study, some amygdala neurons responded to particular emotional expressions even when the visual or auditory element was removed from the original stimuli and maintained the stimulus-preference profile. Our data demonstrate that the same group of neurons is activated when a monkey sees the facial expression of a scream or hears the vocal expression of a scream. The supramodal representation of emotion by these amygdala neurons is useful for receiving the same information about fear from either the face or voice. Our hypothesis is supported by previous human studies. The human amygdala responds to fearful faces and fearful voices, but not to happy or disgusted faces and voices (Dolan et al. 2001; Phillips et al. 1998). Damage to the amygdala can impair the recognition of fearful faces and voices (Adolphs et al. 1994; Scott et al. 1997; Young et al. 1995). Together with these human data, our data indicate that the same amygdala neurons function in receiving information regarding facial and vocal emotions.
In addition to the interesting characteristic of some amygdala neurons, neurons exhibiting supramodal responses were mainly found in the central nucleus of the amygdala, which sends its outputs to other brain areas that are closely related to the production of emotional responses, such as the thalamus, hypothalamus, and brain stem (Amaral et al. 1992; Pitkänen et al. 1997). In contrast, we could not find such neurons in the basal nucleus and accessory basal nucleus, which sends its outputs to the sensory cortex or striatum (Amaral et al. 1992; Pitkänen et al. 1997). Because amygdala neurons preferentially process information of the scream and monkeys are surely required to produce some quick responses to a strong emotion in a tense situation, such as the scream, the information of such a strong emotion would be sent directly to subcortical structures by the central nucleus of the amygdala rather than to the cortex by the basal and accessory basal nuclei. Thus the supramodal representation of emotion in the central nucleus of the amygdala would be very useful for survival by quickly producing appropriate emotional responses.
One question arises from our data. How are these supramodal responses generated? To date, we have no answer to this question. One possibility is that a supramodal response is generated by the integration of visual and auditory information within the amygdala by intrinsic connections. Supramodal responses were found in the central nucleus, although neurons exhibiting visual or auditory responses were frequently found in the lateral, basal, and accessory basal nuclei (Kuraoka and Nakamura 2006; Leonard et al. 1985; Nakamura et al. 1992; Nishijo et al. 1988), which receive direct and indirect visual and auditory inputs from higher-order sensory cortices (Turner et al. 1980), whereas the central nucleus of the amygdala receives intrinsic projections from all of the other nuclei. Our data strongly suggest this possibility. Another possibility is that a supramodal response is the result of associative learning. The amygdala was also implicated in associative learning (Gallagher 2000). The amygdala neurons rapidly change their activity according to an association formed between unimodal stimuli and rewards or punishments in monkeys (Paton et al. 2006) and in rats (Repa et al. 2001). Recent study also showed that human amygdala is responsive to emotional learning from facial expressions (Hooker et al. 2006). In this study, the monkeys had repeatedly experienced the simultaneous presentation of facial and vocal emotions. In particular, the simultaneous presentation of faces and voices always preceded each unimodal presentation in one session. As mentioned earlier, the monkey brain predominantly processes visual information and the amygdala may respond mainly to facial emotion. Consequently, the neurons in the central nucleus might have acquired responsiveness to vocal emotion. In this study, only one neuron predominantly conveyed auditory information. In addition, a few neurons showed supramodal responses to the camera or gong. The monkeys had never seen these objects nor heard the associated sounds before the experiment. Probably, the monkeys had learned the relationship between the sight and sound of the objects during the experiment. Similarly, we associate a voice with a face through experience in our daily life. Thus our results suggest that neurons in the central nucleus of the amygdala could acquire supramodal responsiveness through experience and use the response property to generate appropriate responses to information regarding either facial or vocal emotion. However, further experiments are necessary to confirm this hypothesis.
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FOOTNOTES |
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Address for reprint requests and other correspondence: K. Nakamura, National Institute of Neuroscience, National Center of Neurology and Psychiatry, 4-1-1 Ogawa-Higashi, Kodaira, Tokyo 187-8502, Japan (E-mail: katsuki{at}ncnp.go.jp)
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REFERENCES |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSREFERENCES |
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