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The Journal of Neuroscience, May 30, 2007, 27(22):5958-5966; doi:10.1523/JNEUROSCI.5218-06.2007

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Behavioral/Systems/Cognitive
Processing of Temporal Unpredictability in Human and Animal Amygdala

Cyril Herry,^1 * Dominik R. Bach,^2 * Fabrizio Esposito,³ Francesco Di Salle,^4,5 Walter J. Perrig,⁶ Klaus Scheffler,⁷ Andreas Lüthi,¹ and Erich Seifritz^2,8

¹Friedrich Miescher Institute for Biomedical Research, 4058 Basel, Switzerland, ²University Hospital of Psychiatry Bern, 3000 Bern, Switzerland, ³Department of Neurological Sciences, University of Naples Federico II, 80127 Naples, Italy, ⁴Department of Neuroscience, University of Pisa, 56126 Pisa, Italy, ⁵Department of Cognitive Neuroscience, University of Maastricht, 6200 Maastricht, The Netherlands, ⁶Institute of Psychology, University of Bern, 3000 Bern, Switzerland, ⁷MR Physics, Department of Medical Radiology, University of Basel, 4031 Basel, Switzerland, and ⁸Department of Psychiatry, University of Basel, 4025 Basel, Switzerland

Correspondence should be addressed to either of the following: Dr.Andreas Lüthi, Friedrich Miescher Institute for Biomedical Research, Maulbeerstrasse 66, CH-4058 Basel, Switzerland, Email: andreas.luthi{at}fmi.ch; or Dr. Erich Seifritz, University Hospital of Psychiatry Bern, Bolligenstrasse 111, CH-3000 Bern, Switzerland, E-mail: Email: seifritz{at}puk.unibe.ch

The amygdala has been studied extensively for its critical role in associative fear conditioning in animals and humans. Noxious stimuli, such as those used for fear conditioning, are most effective in eliciting behavioral responses and amygdala activation when experienced in an unpredictable manner. Here, we show, using a translational approach in mice and humans, that unpredictability per se without interaction with motivational information is sufficient to induce sustained neural activity in the amygdala and to elicit anxiety-like behavior. Exposing mice to mere temporal unpredictability within a time series of neutral sound pulses in an otherwise neutral sensory environment increased expression of the immediate-early gene c-fos and prevented rapid habituation of single neuron activity in the basolateral amygdala. At the behavioral level, unpredictable, but not predictable, auditory stimulation induced avoidance and anxiety-like behavior. In humans, functional magnetic resonance imaging revealed that temporal unpredictably causes sustained neural activity in amygdala and anxiety-like behavior as quantified by enhanced attention toward emotional faces. Our findings show that unpredictability per se is an important feature of the sensory environment influencing habituation of neuronal activity in amygdala and emotional behavior and indicate that regulation of amygdala habituation represents an evolutionary-conserved mechanism for adapting behavior in anticipation of temporally unpredictable events.

Key words: unpredictability; amygdala; anxiety; avoidance; habituation; fMRI

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Received Dec. 2, 2006; revised April 26, 2007; accepted April 26, 2007.

Correspondence should be addressed to either of the following: Dr.Andreas Lüthi, Friedrich Miescher Institute for Biomedical Research, Maulbeerstrasse 66, CH-4058 Basel, Switzerland, Email: andreas.luthi{at}fmi.ch; or Dr. Erich Seifritz, University Hospital of Psychiatry Bern, Bolligenstrasse 111, CH-3000 Bern, Switzerland, E-mail: Email: seifritz{at}puk.unibe.ch

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