Processing of temporal unpredictability in human and animal amygdala.

C. Herry, D. R. Bach, F. Esposito, F. Di Salle, W. J. Perrig, K. Scheffler, A. Luthi, E. Seifritz
Journal of Neuroscience. 2007-05-30; 27(22): 5958-5966
DOI: 10.1523/jneurosci.5218-06.2007

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1. J Neurosci. 2007 May 30;27(22):5958-66.

Processing of temporal unpredictability in human and animal amygdala.

Herry C(1), Bach DR, Esposito F, Di Salle F, Perrig WJ, Scheffler K, Lüthi A,
Seifritz E.

Author information:
(1)Friedrich Miescher Institute for Biomedical Research, 4058 Basel, Switzerland.

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.

DOI: 10.1523/JNEUROSCI.5218-06.2007
PMID: 17537966 [Indexed for MEDLINE]


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