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The Journal of Neuroscience, July 2, 2003, 23(13):5496-5502
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Acid-Sensing Ion Channel 1 Is Localized in Brain Regions with High Synaptic Density and Contributes to Fear Conditioning
John A. Wemmie,1,6,7,8 Candice C. Askwith,3,7 Ejvis Lamani,1 Martin D. Cassell,4,6 John H. Freeman, Jr,5,6 andMichael J. Welsh2,3,6,7 Departments of 1Psychiatry, 2Physiology and Biophysics, 3Internal Medicine, 4Anatomy and Cell Biology, and 5Psychology, and 6Neuroscience Graduate Program and 7Howard Hughes Medical Institute, University of Iowa, Iowa City, Iowa 52242 and 8Department of Veterans Affairs Medical Center, Iowa City, Iowa 52242
The acid-sensing ion channel, ASIC1, contributes to synaptic plasticity in the hippocampus and to hippocampus-dependent spatial memory. To explore the role of ASIC1 in brain, we examined the distribution of ASIC1 protein. Surprisingly, although ASIC1 was present in the hippocampal circuit, it was much more abundant in several areas outside the hippocampus. ASIC1 was enriched in areas with strong excitatory synaptic input such as the glomerulus of the olfactory bulb, whisker barrel cortex, cingulate cortex, striatum, nucleus accumbens, amygdala, and cerebellar cortex. Because ASIC1 levels were particularly high in the amygdala, we focused further on this area. We found that extracellular acidosis elicited a greater current density in amygdala neurons than hippocampal neurons and that disrupting the ASIC1 gene eliminated H+-evoked currents in the amygdala. We also tested the effect of ASIC1 on amygdala-dependent behavior; ASIC1-null mice displayed deficits in cue and context fear conditioning, yet baseline fear on the elevated plus maze was intact. These studies suggest that ASIC1 is distributed to regions supporting high levels of synaptic plasticity and contributes to the neural mechanisms of fear conditioning.
Key words: ASIC1; localization; CNS; fear conditioning; emotion; learning, memory
Received Feb. 11, 2003; revised Apr. 23, 2003; accepted Apr. 23, 2003.
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