If it bleeds, it leads: separating threat from mere negativity.
Most theories of emotion hold that negative stimuli are threatening and aversive. Yet in everyday experiences some negative sights (e.g. car wrecks) attract curiosity, whereas others repel (e.g. a weapon pointed in our face). To examine the diversity in negative stimuli, we employed four classes of visual images (Direct Threat, Indirect Threat, Merely Negative and Neutral) in a set of behavioral and functional magnetic resonance imaging studies. Participants reliably discriminated between the images, evaluating Direct Threat stimuli most quickly, and Merely Negative images most slowly. Threat images evoked greater and earlier blood oxygen level-dependent (BOLD) activations in the amygdala and periaqueductal gray, structures implicated in representing and responding to the motivational salience of stimuli. Conversely, the Merely Negative images evoked larger BOLD signal in the parahippocampal, retrosplenial, and medial prefrontal cortices, regions which have been implicated in contextual association processing. Ventrolateral as well as medial and lateral orbitofrontal cortices were activated by both threatening and Merely Negative images. In conclusion, negative visual stimuli can repel or attract scrutiny depending on their current threat potential, which is assessed by dynamic shifts in large-scale brain network activity.
Athinoula A. Martinos Center for Biomedical Imaging, Department of Radiology, Massachusetts General Hospital, Charlestown, MA 02129, USA, Department of Radiology, Harvard Medical School, Boston, MA, 02115 USA, Department of Psychology, Brandeis University, 415 South Street, Waltham MA 02453-2728, USA, Department of Psychology, The Pennsylvania State University, University Park, PA, 16802-3103 USA, Department of Psychology, 3210 Tolman Hall, University of California, Berkeley, Berkeley, 94720 CA, USA, Department of Psychology, 125 Nightingale Hall, Northeastern University, Boston, MA, 02115 USA, Department of Psychiatry, Massachusetts General Hospital, Charlestown, MA, 02129 USA, and Gonda Multidisciplinary Brain Research Center, Building 901, Bar-Ilan University, Ramat Gan, 5290002 Israel Athinoula A. Martinos Center for Biomedical Imaging, Department of Radiology, Massachusetts General Hospital, Charlestown, MA 02129, USA, Department of Radiology, Harvard Medical School, Boston, MA, 02115 USA, Department of Psychology, Brandeis University, 415 South Street, Waltham MA 02453-2728, USA, Department of Psychology, The Pennsylvania State University, University Park, PA, 16802-3103 USA, Department of Psychology, 3210 Tolman Hall, University of California, Berkeley, Berkeley, 94720 CA, USA, Department of Psychology, 125 Nightingale Hall, Northeastern University, Boston, MA, 02115 USA, Department of Psychiatry, Massachusetts General Hospital, Charlestown, MA, 02129 USA, and Gonda Multidisciplinary Brain Research Center, Building 901, Bar-Ilan University, Ramat Gan, 5290002 Israel kestas@nmr.mgh.harvard.edu.
Kestutis
K
Kveraga
Athinoula A. Martinos Center for Biomedical Imaging, Department of Radiology, Massachusetts General Hospital, Charlestown, MA 02129, USA, Department of Radiology, Harvard Medical School, Boston, MA, 02115 USA, Department of Psychology, Brandeis University, 415 South Street, Waltham MA 02453-2728, USA, Department of Psychology, The Pennsylvania State University, University Park, PA, 16802-3103 USA, Department of Psychology, 3210 Tolman Hall, University of California, Berkeley, Berkeley, 94720 CA, USA, Department of Psychology, 125 Nightingale Hall, Northeastern University, Boston, MA, 02115 USA, Department of Psychiatry, Massachusetts General Hospital, Charlestown, MA, 02129 USA, and Gonda Multidisciplinary Brain Research Center, Building 901, Bar-Ilan University, Ramat Gan, 5290002 Israel Athinoula A. Martinos Center for Biomedical Imaging, Department of Radiology, Massachusetts General Hospital, Charlestown, MA 02129, USA, Department of Radiology, Harvard Medical School, Boston, MA, 02115 USA, Department of Psychology, Brandeis University, 415 South Street, Waltham MA 02453-2728, USA, Department of Psychology, The Pennsylvania State University, University Park, PA, 16802-3103 USA, Department of Psychology, 3210 Tolman Hall, University of California, Berkeley, Berkeley, 94720 CA, USA, Department of Psychology, 125 Nightingale Hall, Northeastern University, Boston, MA, 02115 USA, Department of Psychiatry, Massachusetts General Hospital, Charlestown, MA, 02129 USA, and Gonda Multidisciplinary Brain Research Center, Building 901, Bar-Ilan University, Ramat Gan, 5290002 Israel.
Jasmine
J
Boshyan
Athinoula A. Martinos Center for Biomedical Imaging, Department of Radiology, Massachusetts General Hospital, Charlestown, MA 02129, USA, Department of Radiology, Harvard Medical School, Boston, MA, 02115 USA, Department of Psychology, Brandeis University, 415 South Street, Waltham MA 02453-2728, USA, Department of Psychology, The Pennsylvania State University, University Park, PA, 16802-3103 USA, Department of Psychology, 3210 Tolman Hall, University of California, Berkeley, Berkeley, 94720 CA, USA, Department of Psychology, 125 Nightingale Hall, Northeastern University, Boston, MA, 02115 USA, Department of Psychiatry, Massachusetts General Hospital, Charlestown, MA, 02129 USA, and Gonda Multidisciplinary Brain Research Center, Building 901, Bar-Ilan University, Ramat Gan, 5290002 Israel.
Reginald B
RB
Adams
Athinoula A. Martinos Center for Biomedical Imaging, Department of Radiology, Massachusetts General Hospital, Charlestown, MA 02129, USA, Department of Radiology, Harvard Medical School, Boston, MA, 02115 USA, Department of Psychology, Brandeis University, 415 South Street, Waltham MA 02453-2728, USA, Department of Psychology, The Pennsylvania State University, University Park, PA, 16802-3103 USA, Department of Psychology, 3210 Tolman Hall, University of California, Berkeley, Berkeley, 94720 CA, USA, Department of Psychology, 125 Nightingale Hall, Northeastern University, Boston, MA, 02115 USA, Department of Psychiatry, Massachusetts General Hospital, Charlestown, MA, 02129 USA, and Gonda Multidisciplinary Brain Research Center, Building 901, Bar-Ilan University, Ramat Gan, 5290002 Israel.
Jasmine
J
Mote
Athinoula A. Martinos Center for Biomedical Imaging, Department of Radiology, Massachusetts General Hospital, Charlestown, MA 02129, USA, Department of Radiology, Harvard Medical School, Boston, MA, 02115 USA, Department of Psychology, Brandeis University, 415 South Street, Waltham MA 02453-2728, USA, Department of Psychology, The Pennsylvania State University, University Park, PA, 16802-3103 USA, Department of Psychology, 3210 Tolman Hall, University of California, Berkeley, Berkeley, 94720 CA, USA, Department of Psychology, 125 Nightingale Hall, Northeastern University, Boston, MA, 02115 USA, Department of Psychiatry, Massachusetts General Hospital, Charlestown, MA, 02129 USA, and Gonda Multidisciplinary Brain Research Center, Building 901, Bar-Ilan University, Ramat Gan, 5290002 Israel.
Nicole
N
Betz
Athinoula A. Martinos Center for Biomedical Imaging, Department of Radiology, Massachusetts General Hospital, Charlestown, MA 02129, USA, Department of Radiology, Harvard Medical School, Boston, MA, 02115 USA, Department of Psychology, Brandeis University, 415 South Street, Waltham MA 02453-2728, USA, Department of Psychology, The Pennsylvania State University, University Park, PA, 16802-3103 USA, Department of Psychology, 3210 Tolman Hall, University of California, Berkeley, Berkeley, 94720 CA, USA, Department of Psychology, 125 Nightingale Hall, Northeastern University, Boston, MA, 02115 USA, Department of Psychiatry, Massachusetts General Hospital, Charlestown, MA, 02129 USA, and Gonda Multidisciplinary Brain Research Center, Building 901, Bar-Ilan University, Ramat Gan, 5290002 Israel.
Noreen
N
Ward
Athinoula A. Martinos Center for Biomedical Imaging, Department of Radiology, Massachusetts General Hospital, Charlestown, MA 02129, USA, Department of Radiology, Harvard Medical School, Boston, MA, 02115 USA, Department of Psychology, Brandeis University, 415 South Street, Waltham MA 02453-2728, USA, Department of Psychology, The Pennsylvania State University, University Park, PA, 16802-3103 USA, Department of Psychology, 3210 Tolman Hall, University of California, Berkeley, Berkeley, 94720 CA, USA, Department of Psychology, 125 Nightingale Hall, Northeastern University, Boston, MA, 02115 USA, Department of Psychiatry, Massachusetts General Hospital, Charlestown, MA, 02129 USA, and Gonda Multidisciplinary Brain Research Center, Building 901, Bar-Ilan University, Ramat Gan, 5290002 Israel Athinoula A. Martinos Center for Biomedical Imaging, Department of Radiology, Massachusetts General Hospital, Charlestown, MA 02129, USA, Department of Radiology, Harvard Medical School, Boston, MA, 02115 USA, Department of Psychology, Brandeis University, 415 South Street, Waltham MA 02453-2728, USA, Department of Psychology, The Pennsylvania State University, University Park, PA, 16802-3103 USA, Department of Psychology, 3210 Tolman Hall, University of California, Berkeley, Berkeley, 94720 CA, USA, Department of Psychology, 125 Nightingale Hall, Northeastern University, Boston, MA, 02115 USA, Department of Psychiatry, Massachusetts General Hospital, Charlestown, MA, 02129 USA, and Gonda Multidisciplinary Brain Research Center, Building 901, Bar-Ilan University, Ramat Gan, 5290002 Israel.
Nouchine
N
Hadjikhani
Athinoula A. Martinos Center for Biomedical Imaging, Department of Radiology, Massachusetts General Hospital, Charlestown, MA 02129, USA, Department of Radiology, Harvard Medical School, Boston, MA, 02115 USA, Department of Psychology, Brandeis University, 415 South Street, Waltham MA 02453-2728, USA, Department of Psychology, The Pennsylvania State University, University Park, PA, 16802-3103 USA, Department of Psychology, 3210 Tolman Hall, University of California, Berkeley, Berkeley, 94720 CA, USA, Department of Psychology, 125 Nightingale Hall, Northeastern University, Boston, MA, 02115 USA, Department of Psychiatry, Massachusetts General Hospital, Charlestown, MA, 02129 USA, and Gonda Multidisciplinary Brain Research Center, Building 901, Bar-Ilan University, Ramat Gan, 5290002 Israel Athinoula A. Martinos Center for Biomedical Imaging, Department of Radiology, Massachusetts General Hospital, Charlestown, MA 02129, USA, Department of Radiology, Harvard Medical School, Boston, MA, 02115 USA, Department of Psychology, Brandeis University, 415 South Street, Waltham MA 02453-2728, USA, Department of Psychology, The Pennsylvania State University, University Park, PA, 16802-3103 USA, Department of Psychology, 3210 Tolman Hall, University of California, Berkeley, Berkeley, 94720 CA, USA, Department of Psychology, 125 Nightingale Hall, Northeastern University, Boston, MA, 02115 USA, Department of Psychiatry, Massachusetts General Hospital, Charlestown, MA, 02129 USA, and Gonda Multidisciplinary Brain Research Center, Building 901, Bar-Ilan University, Ramat Gan, 5290002 Israel Athinoula A. Martinos Center for Biomedical Imaging, Department of Radiology, Massachusetts General Hospital, Charlestown, MA 02129, USA, Department of Radiology, Harvard Medical School, Boston, MA, 02115 USA, Department of Psychology, Brandeis University, 415 South Street, Waltham MA 02453-2728, USA, Department of Psychology, The Pennsylvania State University, University Park, PA, 16802-3103 USA,
Moshe
M
Bar
Athinoula A. Martinos Center for Biomedical Imaging, Department of Radiology, Massachusetts General Hospital, Charlestown, MA 02129, USA, Department of Radiology, Harvard Medical School, Boston, MA, 02115 USA, Department of Psychology, Brandeis University, 415 South Street, Waltham MA 02453-2728, USA, Department of Psychology, The Pennsylvania State University, University Park, PA, 16802-3103 USA, Department of Psychology, 3210 Tolman Hall, University of California, Berkeley, Berkeley, 94720 CA, USA, Department of Psychology, 125 Nightingale Hall, Northeastern University, Boston, MA, 02115 USA, Department of Psychiatry, Massachusetts General Hospital, Charlestown, MA, 02129 USA, and Gonda Multidisciplinary Brain Research Center, Building 901, Bar-Ilan University, Ramat Gan, 5290002 Israel Athinoula A. Martinos Center for Biomedical Imaging, Department of Radiology, Massachusetts General Hospital, Charlestown, MA 02129, USA, Department of Radiology, Harvard Medical School, Boston, MA, 02115 USA, Department of Psychology, Brandeis University, 415 South Street, Waltham MA 02453-2728, USA, Department of Psychology, The Pennsylvania State University, University Park, PA, 16802-3103 USA, Department of Psychology, 3210 Tolman Hall, University of California, Berkeley, Berkeley, 94720 CA, USA, Department of Psychology, 125 Nightingale Hall, Northeastern University, Boston, MA, 02115 USA, Department of Psychiatry, Massachusetts General Hospital, Charlestown, MA, 02129 USA, and Gonda Multidisciplinary Brain Research Center, Building 901, Bar-Ilan University, Ramat Gan, 5290002 Israel Athinoula A. Martinos Center for Biomedical Imaging, Department of Radiology, Massachusetts General Hospital, Charlestown, MA 02129, USA, Department of Radiology, Harvard Medical School, Boston, MA, 02115 USA, Department of Psychology, Brandeis University, 415 South Street, Waltham MA 02453-2728, USA, Department of Psychology, The Pennsylvania State University, University Park, PA, 16802-3103 USA,
Lisa F
LF
Barrett
D000328:Adult; D000339:Affect / Q000502:physiology*; D001143:Arousal / Q000502:physiology; D001921:Brain / Q000033:anatomy & histology / Q000502:physiology; D001931:Brain Mapping; D004192:Discrimination, Psychological / Q000502:physiology; D004644:Emotions / Q000502:physiology*; D005106:Exploratory Behavior; D005239:Fear / Q000502:physiology; D005260:Female; D006801:Humans; D008279:Magnetic Resonance Imaging; D008297:Male; D008875:Middle Aged; D009042:Motivation; D010100:Oxygen / Q000097:blood; D010775:Photic Stimulation; D055815:Young Adult
D010100:Oxygen
affect; arousal; emotion; fMRI; scenes; valence