The human amygdala plays an important role in gaze monitoring

A PET study
1. 2. 3. 4. 5. 6. 7. 8. 9. Ryuta Kawashima1,2, Motoaki Sugiura1, Takashi Kato3, Akinori Nakamura3, Kentaro Hatano3, Kengo Ito3, Hiroshi Fukuda1,2, Shozo Kojima4 and Katsuki Nakamura4
+ Author Affiliations

1.

1. 1IDAC, Tohoku University, 2. 2Aoba Brain Imaging Reseach Center, Sendai, 3. 3National Institute for Longevity Sciences, Obu and 4. 4Primate Research Institute, Kyoto University, Inuyama, Japan Dr. R. Kawashima, Department of Nuclear Medicine and Radiology, IDAC, Tohoku University, 41 Seiryocho, Aobaku, Sendai, 9808575 Japan E-mail: ryuta@idac.tohoku.ac.jp Received September 4, 1998. Revision received October 14, 1998. Revision received November 12, 1998. Accepted November 24, 1998. Next Section

Summary Social contact often initially depends on ascertaining the direction of the other person's gaze. We determined the brain areas involved in gaze monitoring by a functional neuroimaging study. Discrimination between the direction of gaze significantly activated a region in the left amygdala during eye-contact and no eye-contact tasks to the same extent. However, a region in the right amygdala was specifically activated only during the eye-contact task. Results confirm that the left amygdala plays a general role in the interpretation of eye gaze direction, and that the activity of the right amygdala of the subject increases when another individual's gaze is directed towards him. This suggests that the human amygdala plays a role in reading social signals from the face.
Key words

PET

regional cerebral blood flow

amygdala gaze direction discrimination

social contact

Key words

ANCOVA = analysis of covariance

rCBF = regional cerebral blood flow

SPM = statistical parametric map Previous SectionNext Section

Introduction Humans, but not other primates, have the ability of making inferences about another individual's state of mind (Premack and Woodruff, 1978). Determination of the direction of the other person's gaze is essential for such inferences, as is the observation of another person's eyes for the judgment of his mental state (Baron-Cohen, 1995; Kobayashi and Kohshima, 1997). Neural mechanisms underlying these processes have been investigated by neurophysiological and lesion studies in monkeys which suggest that the superior temporal sulcus area (Rolls, 1984) and amygdala (Leonard et al., 1985) are involved in the determination of the direction of gaze. Autistic patients often exhibit impaired judgement of gaze direction and mental state (Courchesne, 1997) and neuropathological studies have indicated abnormalities of the amygdala, leading to the hypothesis that damage of the amygdala is related to the development of the autistic syndrome (Hoon and Reiss, 1992;Courchesne, 1997). However, data regarding the role of the amygdala in humans have largely been confined to emotion-processing (Gloor, 1990;Adolphs et al., 1994; Cahill et al., 1996; Zald and Pardo, 1997; LaBar et al., 1998; Morris et al., 1998a, b; Whalen et al., 1998), and the neural mechanisms underlying social judgment of other individuals, such as the determination of gaze direction and reading of gaze, are largely unknown.
Previous SectionNext Section

Methods
Subjects

Eight right-handed male volunteers (aged 2053 years) participated in the present study. Written informed consent was obtained from each subject on forms approved by the ethical committee of National Institute for Longevity Sciences and the Declaration of Helsinki (1975). All the subjects were healthy, with no past history of psychiatric or neurological illness, and none was on any medication. High resolution MRI of the brain was performed for each subject.
Task procedures

The experimental task in our study contained three different conditions (Fig. 1). Digitized cinematic images of a woman's face against a uniform background, tilted 30 rightwards from the front, were presented on the same location through a head-mounted display (Mediamask; Olympus, Tokyo, Japan) for all the conditions. In the eyecontact condition, the woman's gaze was directed towards the eyes of a subject who sat just behind the video camera, and then moved randomly either upwards or downwards for a random duration of time (mean 2000 ms; range 15002500 ms). After she had looked upwards or downwards, her gaze returned to the eye-contact position. Subjects were instructed as follows: `Imagine she is looking at you. If you feel her gaze is directed at your head or trunk, press a key with the index finger or middle finger of your right hand, respectively.' The subjects, at an interview after the PET scans, said that they felt that the woman had looked directly at them, and that her attention had been directed towards them during the eye-contact condition. In the no eye-contact condition, the woman's gaze was directed towards a subject who sat next to the video camera, and then she moved her eyes in the same manner as for the eye-contact condition. In this case, the subjects were instructed as follows: `Imagine she is looking at someone who is on your left. If you feel her gaze is directed at that person's head or trunk, press a key with the index finger or middle finger of your right hand, respectively.' The difference between the two eyedirection discrimination conditions was in the direction of gaze of the woman in the image, whether it was directed towards the subjects themselves (the eye-contact condition) or not (the no eye-contact condition), while all other details were exactly the same. In the control condition, her right or left eye winked for a random duration (mean 2000 ms; range 15002500 ms) in a random order. Subjects were instructed to press a key with either the index finger or middle finger of their right hand when her left or right eye winked, respectively (Fig. 1). Under all conditions, the subjects were instructed to attend to the eyes of the presented image, and perform discrimination tasks on the basis of the information obtained from the speed and direction of eye motion and the shape of the eyelids. A digital video recording was made for subsequent analysis of each subject's performance, and the reaction time was determined by frame-by-frame analysis. An electro-oculogram was also recorded for each subject during the PET measurements.
PET

The regional cerebral blood flow (rCBF) was measured using a Siemens ECAT EXACT HR PET scanner in 3D mode, after a bolus injection of H215O (15 mCi per scan). Attenuation-corrected data were reconstructed into 47 image planes with a resulting resolution of 6 mm at full-width half-maximum. All tasks were started immediately after the bolus injection. Each PET measurement was commenced immediately after radioactive counts were identified on the PET camera, and was continued for a period of 90 s. In the present study, one PET scan was obtained for each task. The order of the three tasks was counterbalanced across the subjects.
Image data analysis

A human brain atlas system (Roland et al., 1994) was used for image realignment and transformation into standard stereotaxic space. Then statistical parametric mapping (SPM96, Wellcome Department of Cognitive Neurology, London) software was used for smoothing and statistical analysis (Friston et al., 1995). In this study, an isotropic Gaussian filter with a full-width half-maximum of 12 mm was used to increase the signal-to-noise ratio and to compensate for individual differences in gyral anatomy. Differences in global flow were analysed using ANCOVA (analysis of covariance). Comparisons across conditions were made by means of t-statistics, and thereafter transformed into normally distributedZ-statistics. In the case of the amygdala, for which we had a region-specific hypothesis, correction for multiple comparisons was based on the size of the amygdala as done by others (Breiter et al., 1996; Whalen et al., 1998) and the smoothness of the underlying SPM (Worsley et al., 1996). For the rest of the brain, where we had no a priori regional hypothesis, correction was made for the entire volume analysed. Thus, in all cases the threshold for significant activation was set at P < 0.05 (corrected). Finally, each area of activation was superimposed on to the average transformed MRI of the same eight subjects involved in this study. Anatomical localization of areas of activation in each comparison was made in relation to the mean anatomically standardized MRI, since the standard brain of the human brain atlas has a size and shape different from that of SPM96 and is also situated in a slightly different stereotaxic coordinate system from that of Talairach and Tournoux (1988).
Previous SectionNext Section

Results
Behaviour

Electro-oculogram recordings showed no evidence of saccadic eye movements during any task. The mean (standard deviation) response times were 438 (31), 408 (31) and 398 (31) ms during the eye-contact, no eyecontact and control conditions, respectively.
Brain activation

Eye-direction discrimination tasks during the eye-contact condition activated the amygdala bilaterally (P < 0.05, corrected for multiple comparisons) when compared with the control condition (Fig. 2). The corresponding area in the left amygdala was activated to the same extent (P < 0.05, corrected for multiple comparisons) during the no eye-contact condition (Fig. 2) as during the eye-contact condition (Fig. 3) when compared with the control condition. The right amygdala, however, did not show any increase in neural activity during the no eye-contact condition (Fig. 3). This field shows increases in rCBF during the eye-contact condition when compared with the no eye-contact condition (P < 0.003, uncorrected). In addition, areas in the left insula (Fig. 4A) and posterior cingulate cortex (Fig. 4B) showed increases in rCBF during the eye-contact condition when compared with the control condition. Activation in these fields did not reach statistical significance (P < 0.05, corrected) although it did achieve an uncorrected significance level of P < 0.001. The stereotactic coordinates of rCBF changes according to the atlas of Talairach and Tournoux (1988) are given in Table 1. These two fields also showed increases in the rCBF when compared with the no eye-contact condition (P < 0.001, uncorrected). Deactivation was not observed for either the eye-contact or the no eye-contact condition when compared with the control condition.
Previous SectionNext Section

Discussion The experimental protocol was designed such that significant activation as evaluated by both eye-contact condition versus control and no eye-contact condition versus control comparisons reflected the neural responses involved in determining the eye gaze direction, and that significant increases in rCBF during the eye-contact condition compared with either the no eye-contact or control conditions identified areas activated specifically when another individual's gaze is directed towards the subject (Keating and Keating, 1982; Baron-Cohen, 1995).

Our results indicate that the human amygdala plays a role in reading social signals from the face (Leonard et al., 1985; Heywood and Cowey, 1992; Nakamuraet al., 1992; Seeck et al., 1993; Young et al., 1995). Recent neuroimaging studies in humans have demonstrated activation within the amygdala in response to overt (Adolphs et al., 1994; Morris et al., 1996, 1998a) or masked (Morris et al., 1998b; Whalen et al., 1998) emotionally expressive faces, or to arousal, threatening or fear-provoking stimuli (Gloor, 1990; Cahill et al., 1996; Zald and Pardo, 1997; LaBar et al., 1998). These data regarding the role of the amygdala in humans have been confined to emotion-processing. In these studies, the gazes of both emotionally expressive and control neutral faces used as stimuli were directed towards the subjects. Although subjects probably responded to the emotional expression in the eyes of the objectives, the amygdala activation in these studies could not be related to the direction of gaze. To our knowledge, this is the first brain imaging study investigating the involvement of the human amygdala in social judgement of other individuals on the basis of their eye gaze direction. Our findings are consistent with the results of neurophysiological studies in monkeys which demonstrated that the medial and lateral nuclei of the amygdala have cells sensitive to eye direction (Brothers et al., 1990), as well as human lesion studies investigating impairment of gaze direction interpretation after amygdalotomy (Young et al., 1995; Adolphs et al., 1998). They support the hypothesis proposing a role for the amygdala in social behavior (Dicks et al., 1968; Brothers et al., 1990; Adolphs et al., 1998). Although, the area most closely related to determination of the gaze direction was found in the superior temporal sulcus in neurophysiological (Perrett et al., 1985) and lesion (Campbell et al., 1990) studies in monkeys, we did not find any significant activation in this region. This could well be due to activation of the superior temporal sulcus region during the control condition, in which subjects were required to attend to the presented images of the face, since the neurons in this region have been shown to respond primarily to faces (Rolls et al., 1992). In the present study, eye-contact condition-specific activation was observed not only in the right amygdala but also in other areas in the limbic system, namely, the left insula and cingulate cortex. Human studies have suggested that limbic structures may respond more to stimuli that directly induce strong emotional responses (Adolphs et al., 1994; Morriset al., 1996; Phillips et al., 1997). Since we used cinematic images of faces as visual stimuli, three objectives in all the three conditions had some emotional expression. However, in human social life, it is reasonable to assume that most people would be hypersensitive to another person watching them (BaronCohen, 1995). We therefore suggest that the activation of these structures in the limbic system is related to the strong emotional responses evoked during the eye-contact task.

Table 1
View this table: In this window In a new window

Locations of increased blood flow during eye direction discrimination tasks

View larger version:

In this page In a new window

Fig. 1

Download as PowerPoint Slide

Visual stimuli used for the eye-contact (upper column), no eye-contact (middle column) and control (lower column) conditions. Subjects were asked to judge whether the eyes were directed upwards or downwards during the eye-contact and no eye-contact conditions, and whether the left or right eye blinked during the control condition.

View larger version:

In this page In a new window

Fig. 2

Download as PowerPoint Slide

Horizontal (left) and coronal (right) sections of the mean spatially-normalized MRI (grey scale) through peak activation of the amgydala as evaluated in the eye-contact versus control (upper) and the no eye-contact versus control (lower) comparisons. Red areas on the MRI show the field of activation. The left sides of the figures correspond to the left hemisphere.

View larger version:

In this page In a new window

Fig. 3

Download as PowerPoint Slide

Mean normalized rCBF values in ml/100 g/min during the eye-direction discrimination and control conditions are shown from voxels showing peak activation in the left and right amygdala. Error bars indicate standard deviation.

View larger version:

In this page In a new window

Fig. 4

Download as PowerPoint Slide

Horizontal (left) and coronal (right) sections of the mean spatially-normalized MRI (grey scale) through peak activation of the left insula (A) and posterior cingulate cortex (B) as evaluated in the eye-contact versus control comparison. Red areas on the MRI show the field of activation.
Previous SectionNext Section

Acknowledgments

We wish to thank Professor P. E. Roland for his advice on the manuscript and Ms A. Watanabe for technical assistance. This research was supported by Grants-in-Aid for Scientific Research on Priority Research from the Japanese Ministry of Education, Science, Sports and Culture (10164206, 09207102) and Research for the Future from Japan Society for the Promotion of Science (JSPS-RFTF 97L00202).

Oxford University Press 1999 Previous Section

References
1.

Adolphs R, Tranel D, Damasio H, Damasio A. Impaired recognition of emotion in facial expressions following bilateral damage to the human amygdala [see comments].Nature 1994; 372: 66972. Comment in: Nature 1994; 372: 6134.
CrossRefMedline

2.

Adolphs R, Tranel D, Damasio AR. The human amygdala in social judgment. Nature1998; 393: 4704. Comment in: Nature 1998; 393: 4178
CrossRefMedline

3. 4.

Baron-Cohen S. Mindblindness: An essay on autism and theory of mind. Cambridge (MA): MIT Press; 1995.

Breiter HC, Etcoff NL, Whalen PJ, Kennedy WA, Rauch SL, Buckner RL, et al. Response and habituation of the human amygdala during visual processing of facial expression. Neuron 1996; 17: 87587.
CrossRefMedlineWeb of Science

5.

Brothers L, Ring B, Kling A. Response of neurons in the macaque amygdala to complex social stimuli. Behav Brain Res 1990; 41: 199213.
CrossRefMedlineWeb of Science

6.

Cahill L, Haier RJ, Fallon J, Alkire MT, Tang C, Keator D, et al. Amygdala activity at encoding correlated with long-term, free recall of emotional information. Proc Natl Acad Sci USA 1996; 93: 801621.
Abstract/FREE Full Text

7.

Campbell R, Heywood CA, Cowey A, Regard M, Landis T. Sensitivity to eye gaze in prosopagnosic patients and monkeys with superior temporal sulcus ablation.Neuropsychologia 1990; 28: 112342.
CrossRefMedlineWeb of Science

8.

Courchesne E. Brainstem, cerebellar and limbic neuroanatomical abnormalities in autism [published erratum appears in Curr Opin Neurobiol 1997; 7: S68]. [Review].Curr Opin Neurobiol 1997; 7: 26978.
CrossRefMedlineWeb of Science

9.

Dicks D, Myers RE, Kling A. Uncus and amygdala lesions: effects on social behavior in the free-ranging rhesus monkey. Science 1968; 165: 6971.

10.

Friston KJ, Holmes AP, Worsley KJ, Poline J-B, Frith CD, Frackowiak RSJ. Statistical parametric maps in functional imaging: a general linear approach. Hum Brain Mapp1995; 2: 189210.
CrossRef

11.

Gloor P. Experimental phenomena of temporal lobe epilepsy. Facts and hypotheses. [Review]. Brain 1990; 113: 167394.
Abstract/FREE Full Text

12.

Heywood CA, Cowey A. The role of the `face-cell' area in the discrimination and recognition of faces by monkeys. Philos Trans R Soc Lond B Biol Sci 1992; 335: 318.
Abstract/FREE Full Text

13.

Hoon AH Jr, Reiss AL. The mesial-temporal lobe and autism: case report and review. [Review]. Dev Med Child Neurol 1992; 34: 2529.
MedlineWeb of Science

14.

Keating CF, Keating EG. Visual scan patterns of rhesus monkeys viewing faces.Perception 1982; 11: 2119.
MedlineWeb of Science

15.

Kobayashi H, Kohshima S. Unique morphology of the human eye [letter]. Nature1997; 387: 7678.
Medline

16.

LaBar KS, Gatenby JC, Gore JC, LeDoux JE, Phelps EA. Human amygdala activation during conditioned fear acquisition and extinction: a mixed-trial fMRI study. Neuron1998; 20: 93745.
CrossRefMedlineWeb of Science

17.

Leonard CM, Rolls ET, Wilson FA, Baylis GC. Neurons in the amygdala of the monkey with responses selective for faces. Behav Brain Res 1985; 15: 159176.
CrossRefMedlineWeb of Science

18.

Morris JS, Frith CD, Perrett DI, Rowland D, Young AW, Calder AJ, et al. A differential neural response in the human amygdala to fearful and happy facial expressions. Nature1996; 383: 8125.
CrossRefMedline

19.

Morris JS, Friston KJ, Buchel C, Frith CD, Young AW, Calder AJ, et al. A neuromodulatory role for the human amygdala in processing emotional facial expressions. Brain 1998a; 121: 4757.
Abstract/FREE Full Text

20.

Morris JS, Ohman A, Dolan RJ. Conscious and unconscious emotional learning in the human amygdala [see comments]. Nature 1998b; 393:46770. Comment in: Nature 1998b; 393: 4178.
CrossRefMedline

21.

Nakamura K, Mikami A, Kubota K. Activity of single neurons in the monkey amygdala during performance of a visual discrimination task. J Neurophysiol 1992; 67:144863.

22.

Perrett DI, Smith PAJ, Potter DD, Mistlin AJ, Head AS, Milner AD, et al. Visual cells in the temporal cortex sensitive to face view and gaze direction. Proc R Soc Lond B Biol Sci1985; 223: 293317.
Medline

23.

Phillips ML, Young AW, Senior C, Brammer M, Andrew C, Calder AJ, et al. A specific neural substrate for perceiving facial expressions of disgust. Nature 1997; 389: 4958.
CrossRefMedline

24.

Premack D, Woodruff G. Does the chimpanzee have a theory of mind? Behav Brain Sci 1978; 4: 51526.
CrossRef

25.

Roland PE, Graufelds CJ, Wahlin J, Ingelman L, Andersson M, Ledberg A, et al. Human brain atlas: for high-resolution functional and anatomical mapping. Hum Brain Mapp 1994; 1: 17384.
CrossRef

26.

Rolls ET. Neurons in the cortex of the temporal lobe and in the amygdala of the monkey with responses selective for faces. Hum Neurobiol 1984; 3: 20922.
MedlineWeb of Science

27. Rolls ET. Neurophysiological mechanisms underlying face processing within and beyond the temporal cortical visual areas.
[Review]. Philos Trans R Soc Lond B Biol Sci 1992;335: 1120.
Abstract/FREE Full Text

28.

Seeck M, Mainwaring N, Ives J, Blume H, Dubuisson D, Cosgrove R, et al. Differential neural activity in the human temporal lobe evoked by faces of family members and friends. Ann Neurol 1993; 34: 36972.
CrossRefMedlineWeb of Science

29. Talairach J, Tournoux P. Co-planar stereotaxic atlas of the human brain. Stuttgart: Thieme; 1988. 30.
Whalen PJ, Rauch SL, Etcoff NL, McInerney SC, Lee MB, Jenile MA. Masked presentations of emotional facial expressions modulate amygdala activity without explicit knowledge. J Neurosci 1998; 18: 41118.
Abstract/FREE Full Text

31.

Worsley KJ, Marrett S, Neelin P, Evans AC. Searching scale space for activation in PET images. Hum Brain Mapp 1996; 4: 7490.
CrossRefMedlineWeb of Science

32.

Young AW, Aggleton JP, Hellawell DJ, Johnson M, Broks P, Hanley JR. Face processing impairments after amygdalotomy. Brain 1995; 118: 1524.
Abstract/FREE Full Text

33.

Zald DH, Pardo JV. Emotion, olfaction, and the human amygdala: amygdala activation during aversive olfactory stimulation. Proc Natl Acad Sci USA 1997; 94: 411924.
Abstract/FREE Full Text

Articles citing this article

o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o
Effects of gaze direction, head orientation and valence of facial expression on amygdala activitySoc Cogn Affect
Neurosci (2013) 0 (2013): nst100v2-nst100

Abstract Full Text (HTML) Full Text (PDF) Feature-based representations of emotional facial expressions in the human amygdalaSoc Cogn Affect Neurosci (2013) 0 (2013): nst112v2-nst112 Abstract Full Text (HTML) Full Text (PDF) Placebo and the New Physiology of the Doctor-Patient RelationshipPhysiol. Rev. (2013) 93 (3): 1207-1246 Abstract Full Text (HTML) Full Text (PDF) Amygdala Activation for Eye Contact Despite Complete Cortical BlindnessJ. Neurosci. (2013) 33 (25): 10483-10489 Abstract Full Text (HTML) Full Text (PDF) Distinct Contributions to Facial Emotion Perception of Foveated versus Nonfoveated Facial FeaturesEmotion Review (2013) 5 (1): 30-35 Abstract Full Text (HTML) Full Text (PDF) The Role of the Amygdala in Atypical Gaze on Emotional Faces in Autism Spectrum DisordersJ. Neurosci. (2012) 32 (28): 9469-9476 Abstract Full Text (HTML) Full Text (PDF) Eye gaze adaptation under interocular suppressionJ Vis (2012) 12 (7): 1 Abstract Full Text (HTML) Full Text (PDF) Does it make a difference if I have an eye contact with you or with your picture? An ERP studySoc Cogn Affect Neurosci (2011) 6 (4): 486-494 Abstract Full Text (HTML) Full Text (PDF) Connectivity Analysis Reveals a Cortical Network for Eye Gaze PerceptionCereb Cortex (2010) 20 (8): 1780-1787 Abstract Full Text (HTML) Full Text (PDF) Integration of gaze direction and facial expression in patients with unilateral amygdala damageBrain (2010) 133 (1): 248-261 Abstract Full Text (HTML) Full Text (PDF) Amygdala response to faces parallels social behavior in Williams syndromeSoc Cogn Affect Neurosci (2009) 4 (3): 278-285 Abstract Full Text (HTML) Full Text (PDF) Mirroring of attention by neurons in macaque parietal cortexProc. Natl. Acad. Sci. USA (2009) 106 (23): 9489-9494 Abstract Full Text (HTML) Full Text (PDF)

 o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o

Impaired Social Cognition in Mild Alzheimer DiseaseJ Geriatr Psychiatry Neurol (2009) 22 (2): 130-140 Abstract Full Text (PDF) Asymmetries of the human social brain in the visual, auditory and chemical modalitiesPhil Trans R Soc B (2009) 364 (1519): 895-914 Abstract Full Text (HTML) Full Text (PDF) Amygdala activation during reading of emotional adjectives--an advantage for pleasant contentSoc Cogn Affect Neurosci (2009) 4 (1): 35-49 Abstract Full Text (HTML) Full Text (PDF) Time course of superior temporal sulcus activity in response to eye gaze: a combined fMRI and MEG studySoc Cogn Affect
Neurosci (2008) 3 (3): 224-232

Abstract Full Text (HTML) Full Text (PDF) Oxytocin Attenuates Affective Evaluations of Conditioned Faces and Amygdala ActivityJ. Neurosci. (2008) 28 (26): 6607-6615 Abstract Full Text (HTML) Full Text (PDF) Learning affective values for faces is expressed in amygdala and fusiform gyrusSoc Cogn Affect Neurosci (2008) 3 (2): 109-118 Abstract Full Text (HTML) Full Text (PDF) Neurons in the fusiform gyrus are fewer and smaller in autismBrain (2008) 131 (4): 987-999 Abstract Full Text (HTML) Full Text (PDF) Eye-Gaze Direction Modulates Race-Related Amygdala ActivityGroup Processes Intergroup Relations (2008) 11 (2): 233-246 Abstract Full Text (PDF) Involvement of medial temporal structures in reflexive attentional shift by gazeSoc Cogn Affect Neurosci (2008) 3 (1): 80-88 Abstract Full Text (HTML) Full Text (PDF) The left amygdala knows fear: laterality in the amygdala response to fearful eyesSoc Cogn Affect Neurosci (2008) 3 (1): 47-54 Abstract Full Text (HTML) Full Text (PDF) Unilateral Amygdala Lesions Hamper Attentional Orienting Triggered by Gaze DirectionCereb Cortex (2007) 17 (11): 2593-2600 Abstract Full Text (HTML) Full Text (PDF) Gender Specific Processing of Eye Contact within the Human Medial Temporal LobeClin EEG Neurosci (2007) 38 (3): 143-147 Abstract Full Text (HTML) Full Text (PDF) Genetic influences on the neural basis of social cognitionPhil Trans R Soc B (2006) 361 (1476): 2129-2141 Abstract Full Text (HTML) Full Text (PDF)

 o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o o

Brain Networks Involved in Viewing Angry Hands or FacesCereb Cortex (2006) 16 (8): 1087-1096 Abstract Full Text (HTML) Full Text (PDF) Pupillary contagion: central mechanisms engaged in sadness processingSoc Cogn Affect Neurosci (2006) 1 (1): 5-17 Abstract Full Text (HTML) Full Text (PDF) Amygdala fMRI lateralizes temporal lobe epilepsyNeurology (2006) 66 (1): 81-87 Abstract Full Text (HTML) Full Text (PDF) A WORLD OF LIES.Journal of Cross-Cultural Psychology (2006) 37 (1): 60-74 Abstract Full Text (PDF) Individual differences in infant attention skills, joint attention, and emotion regulation behaviourInternational Journal of Behavioral
Development (2005) 29 (3): 259-263

Abstract Full Text (PDF) The Look of Love: Gaze Shifts and Person PerceptionPsychological Science (2005) 16 (3): 236-239 Abstract Full Text (HTML) Full Text (PDF) Neuroimaging in Disorders of Social and Emotional Functioning: What Is the Question?J Child Neurol (2004) 19 (10): 772-784 Abstract Full Text (PDF) When Strangers Pass: Processing of Mutual and Averted Social Gaze in the Superior Temporal SulcusPsychological
Science (2004) 15 (9): 598-603

Abstract Full Text (HTML) Full Text (PDF) The impact of early and late damage to the human amygdala on 'theory of mind' reasoningBrain (2004) 127 (7): 1535-1548 Abstract Full Text (HTML) Full Text (PDF) Dynamic Perception of Facial Affect and Identity in the Human BrainCereb Cortex (2003) 13 (10): 1023-1033 Abstract Full Text (HTML) Full Text (PDF) Are You Looking at Me? Eye Gaze and Person PerceptionPsychological Science (2002) 13 (5): 460-464 Abstract Full Text (PDF) An fMRI study of intentional and unintentional (embarrassing) violations of social normsBrain (2002) 125 (8): 1696-1708 Abstract Full Text (HTML) Full Text (PDF) Recognizing Emotion from Facial Expressions: Psychological and Neurological MechanismsBehav Cogn Neurosci Rev (2002) 1 (1): 21-62 Abstract Full Text (PDF)

 o o o

Face processing occurs outside the fusiform `face area' in autism: evidence from functional MRIBrain (2001) 124 (10): 2059-2073 Abstract Full Text (HTML) Full Text (PDF) Previous | Next Article Table of Contents

This Article
1. 1. 2. 3. 1. 2. 3. 4. 5. 6. 7. 8. 9. AbstractFree Full Text (HTML)Free Full Text (PDF)Free
- Services

Brain (1999) 122 (4): 779-783.doi: 10.1093/brain/122.4.779

Alert me when cited Alert me if corrected Find similar articles Similar articles in Web of Science Similar articles in PubMed Add to my archive Download citation Request Permissions Disclaimer
+ Citing Articles + Google Scholar + PubMed - Share

1. 2.

o o o o o
What's this?

Navigate This Article

1. 2. 3. 4. 5. 6. 7. 8. Top Summary Introduction Methods Results Discussion Acknowledgments References

This Article
1. 1. 2. 3. 1. 2. 3. 4. 5. 6. 7. 8. AbstractFree Full Text (HTML)Free Full Text (PDF)Free Brain (1999) 122 (4): 779-783.doi: 10.1093/brain/122.4.779

Navigate This Article

Top Summary Introduction Methods Results Discussion Acknowledgments References
Search this journal:

Advanced

Current Issue

1.

December 2013 136 (12)

1. 1. Alert me to new issues

The Journal
About this journal Rights & Permissions This journal is a member of the Committee on Publication Ethics (COPE) We are mobile find out more

Published on behalf of
The Guarantors of Brain

Travel Grants, Bursaries and Entry Scholarships

Impact factor: 9.915 5-Yr impact factor: 10.870 Editor

Alastair Compston

View full editorial board

For Authors
Instructions to authors Online submission Submit Now! Self-archiving policy

Open access options for authors - visit Oxford Open

This journal enables compliance with the NIH Public Access Policy

Alerting Services
Email table of contents Email Advance Access CiteTrack XML RSS feed PDA Access

Corporate Services


1. 2.

Advertising sales Reprints Supplements

Widget
Get a widget
Most Read Most Cited

The power of music Transcranial Doppler detected cerebral microembolism following carotid endarterectomy. High microembolic signal loads predict postoperative cerebral ischaemia 3. Pathophysiology of bradykinesia in Parkinson's disease 4. A positron emission tomography study of nigro-striatal dopaminergic mechanisms underlying attention: implications for ADHD and its treatment 5. THE PREFRONTAL CORTEXEXECUTIVE AND COGNITIVE FUNCTIONS. View all Most Read articles Online ISSN 1460-2156 - Print ISSN 0006-8950