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      Context conditioning and extinction in humans: differential contribution of the hippocampus, amygdala and prefrontal cortex

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          Abstract

          Functional magnetic resonance imaging was used to investigate the role of the hippocampus, amygdala and medial prefrontal cortex (mPFC) in a contextual conditioning and extinction paradigm provoking anxiety. Twenty-one healthy persons participated in a differential context conditioning procedure with two different background colours as contexts. During acquisition increased activity to the conditioned stimulus (CS+) relative to the CS− was found in the left hippocampus and anterior cingulate cortex (ACC). The amygdala, insula and inferior frontal cortex were differentially active during late acquisition. Extinction was accompanied by enhanced activation to CS+ vs. CS− in the dorsal anterior cingulate cortex (dACC). The results are in accordance with animal studies and provide evidence for the important role of the hippocampus in contextual learning in humans. Connectivity analyses revealed correlated activity between the left posterior hippocampus and dACC (BA32) during early acquisition and the dACC, left posterior hippocampus and right amygdala during extinction. These data are consistent with theoretical models that propose an inhibitory effect of the mPFC on the amygdala. The interaction of the mPFC with the hippocampus may reflect the context-specificity of extinction learning.

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          Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing

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            Interoception: the sense of the physiological condition of the body.

            Converging evidence indicates that primates have a distinct cortical image of homeostatic afferent activity that reflects all aspects of the physiological condition of all tissues of the body. This interoceptive system, associated with autonomic motor control, is distinct from the exteroceptive system (cutaneous mechanoreception and proprioception) that guides somatic motor activity. The primary interoceptive representation in the dorsal posterior insula engenders distinct highly resolved feelings from the body that include pain, temperature, itch, sensual touch, muscular and visceral sensations, vasomotor activity, hunger, thirst, and 'air hunger'. In humans, a meta-representation of the primary interoceptive activity is engendered in the right anterior insula, which seems to provide the basis for the subjective image of the material self as a feeling (sentient) entity, that is, emotional awareness.
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              Neurons in medial prefrontal cortex signal memory for fear extinction.

              Conditioned fear responses to a tone previously paired with a shock diminish if the tone is repeatedly presented without the shock, a process known as extinction. Since Pavlov it has been hypothesized that extinction does not erase conditioning, but forms a new memory. Destruction of the ventral medial prefrontal cortex, which consists of infralimbic and prelimbic cortices, blocks recall of fear extinction, indicating that medial prefrontal cortex might store long-term extinction memory. Here we show that infralimbic neurons recorded during fear conditioning and extinction fire to the tone only when rats are recalling extinction on the following day. Rats that froze the least showed the greatest increase in infralimbic tone responses. We also show that conditioned tones paired with brief electrical stimulation of infralimbic cortex elicit low freezing in rats that had not been extinguished. Thus, stimulation resembling extinction-induced infralimbic tone responses is able to simulate extinction memory. We suggest that consolidation of extinction learning potentiates infralimbic activity, which inhibits fear during subsequent encounters with fear stimuli.
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                Author and article information

                Journal
                Eur J Neurosci
                ejn
                The European Journal of Neuroscience
                Blackwell Publishing Ltd
                0953-816X
                1460-9568
                February 2009
                : 29
                : 4
                : 823-832
                Affiliations
                [1 ]Department of Clinical and Cognitive Neuroscience, Central Institute of Mental Health, University of Heidelberg Mannheim, Germany
                [2 ]Department of Computer Assisted Clinical Medicine, Faculty of Medicine Mannheim, University of Heidelberg Mannheim, Germany
                Author notes
                Correspondence: Dr H. Flor, as above. E-mail: herta.flor@ 123456zi-mannheim.de
                Article
                10.1111/j.1460-9568.2009.06624.x
                2695154
                19200075
                e2f407fa-c955-44ee-9eb1-694cb6e1d1a2
                Journal compilation © 2009 Federation of European Neuroscience Societies and Blackwell Publishing Ltd

                Re-use of this article is permitted in accordance with the Creative Commons Deed, Attribution 2.5, which does not permit commercial exploitation.

                History
                : 17 September 2008
                : 01 December 2008
                : 14 December 2008
                Categories
                Behavioral Neuroscience

                Neurosciences
                functional connectivity,anxiety,fear learning,functional magnetic resonance imaging (fmri)

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