Preferential attention to animals and people is independent of the amygdala

Shuo Wang; Naotsugu Tsuchiya; Joshua New; Rene Hurlemann; Ralph Adolphs

doi:10.1093/scan/nsu065

Preferential attention to animals and people is independent of the amygdala

Soc Cogn Affect Neurosci. 2015 Mar;10(3):371-80. doi: 10.1093/scan/nsu065. Epub 2014 May 1.

Authors

Shuo Wang¹, Naotsugu Tsuchiya², Joshua New³, Rene Hurlemann³, Ralph Adolphs⁴

Affiliations

¹ Computation and Neural Systems, California Institute of Technology, Pasadena, CA 91125, USA, Decoding and Controlling Brain Information, Japan Science and Technology Agency, Chiyoda-ku, Tokyo 102-0076, Japan, School of Psychological Sciences, Monash University, Clayton, Victoria 3800, Australia, Division of Humanities and Social Sciences, California Institute of Technology, Pasadena, CA 91125, USA, Department of Psychology, Barnard College, Columbia University New York, NY 10027, USA, and Department of Psychiatry, University of Bonn, 53105 Bonn, Germany wangshuo45@gmail.com.
² Computation and Neural Systems, California Institute of Technology, Pasadena, CA 91125, USA, Decoding and Controlling Brain Information, Japan Science and Technology Agency, Chiyoda-ku, Tokyo 102-0076, Japan, School of Psychological Sciences, Monash University, Clayton, Victoria 3800, Australia, Division of Humanities and Social Sciences, California Institute of Technology, Pasadena, CA 91125, USA, Department of Psychology, Barnard College, Columbia University New York, NY 10027, USA, and Department of Psychiatry, University of Bonn, 53105 Bonn, Germany Computation and Neural Systems, California Institute of Technology, Pasadena, CA 91125, USA, Decoding and Controlling Brain Information, Japan Science and Technology Agency, Chiyoda-ku, Tokyo 102-0076, Japan, School of Psychological Sciences, Monash University, Clayton, Victoria 3800, Australia, Division of Humanities and Social Sciences, California Institute of Technology, Pasadena, CA 91125, USA, Department of Psychology, Barnard College, Columbia University New York, NY 10027, USA, and Department of Psychiatry, University of Bonn, 53105 Bonn, Germany Computation and Neural Systems, California Institute of Technology, Pasadena, CA 91125, USA, Decoding and Controlling Brain Information, Japan Science and Technology Agency, Chiyoda-ku, Tokyo 102-0076, Japan, School of Psychological Sciences, Monash University, Clayton, Victoria 3800, Australia, Division of Humanities and Social Sciences, California Institute of Technology, Pasadena, CA 91125, USA, Department of Psychology, Barnard College, Columbia University New York, NY 10027, USA, and Department of Psychiatry, University of Bonn, 53105 Bonn, Germany.
³ Computation and Neural Systems, California Institute of Technology, Pasadena, CA 91125, USA, Decoding and Controlling Brain Information, Japan Science and Technology Agency, Chiyoda-ku, Tokyo 102-0076, Japan, School of Psychological Sciences, Monash University, Clayton, Victoria 3800, Australia, Division of Humanities and Social Sciences, California Institute of Technology, Pasadena, CA 91125, USA, Department of Psychology, Barnard College, Columbia University New York, NY 10027, USA, and Department of Psychiatry, University of Bonn, 53105 Bonn, Germany.
⁴ Computation and Neural Systems, California Institute of Technology, Pasadena, CA 91125, USA, Decoding and Controlling Brain Information, Japan Science and Technology Agency, Chiyoda-ku, Tokyo 102-0076, Japan, School of Psychological Sciences, Monash University, Clayton, Victoria 3800, Australia, Division of Humanities and Social Sciences, California Institute of Technology, Pasadena, CA 91125, USA, Department of Psychology, Barnard College, Columbia University New York, NY 10027, USA, and Department of Psychiatry, University of Bonn, 53105 Bonn, Germany Computation and Neural Systems, California Institute of Technology, Pasadena, CA 91125, USA, Decoding and Controlling Brain Information, Japan Science and Technology Agency, Chiyoda-ku, Tokyo 102-0076, Japan, School of Psychological Sciences, Monash University, Clayton, Victoria 3800, Australia, Division of Humanities and Social Sciences, California Institute of Technology, Pasadena, CA 91125, USA, Department of Psychology, Barnard College, Columbia University New York, NY 10027, USA, and Department of Psychiatry, University of Bonn, 53105 Bonn, Germany.

Abstract

The amygdala is thought to play a critical role in detecting salient stimuli. Several studies have taken ecological approaches to investigating such saliency, and argue for domain-specific effects for processing certain natural stimulus categories, in particular faces and animals. Linking this to the amygdala, neurons in the human amygdala have been found to respond strongly to faces and also to animals. However, the amygdala's necessary role for such category-specific effects at the behavioral level remains untested. Here we tested four rare patients with bilateral amygdala lesions on an established change-detection protocol. Consistent with prior published studies, healthy controls showed reliably faster and more accurate detection of people and animals, as compared with artifacts and plants. So did all four amygdala patients: there were no differences in phenomenal change blindness, in behavioral reaction time to detect changes or in eye-tracking measures. The findings provide decisive evidence against a critical participation of the amygdala in rapid initial processing of attention to animate stimuli, suggesting that the necessary neural substrates for this phenomenon arise either in other subcortical structures (such as the pulvinar) or within the cortex itself.

Keywords: amygdala; attention; change detection; eye-tracking.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Amygdala / pathology
Amygdala / physiopathology*
Animals
Attention / physiology*
Emotions / physiology
Eye Movements
Female
Humans
Lipoid Proteinosis of Urbach and Wiethe / pathology
Lipoid Proteinosis of Urbach and Wiethe / psychology*
Photic Stimulation
Psychomotor Performance
Reaction Time
Visual Perception

Grants and funding

P50 MH094258/MH/NIMH NIH HHS/United States