The Journal of Neuroscience, July 1, 2009, 29(26):8474-8482; doi:10.1523/JNEUROSCI.0378-09.2009
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Behavioral/Systems/Cognitive
Sustained Conditioned Responses in Prelimbic Prefrontal Neurons Are Correlated with Fear Expression and Extinction Failure
Anthony Burgos-Robles, *
Ivan Vidal-Gonzalez, *
and
Gregory J. Quirk
Departments of Psychiatry and Anatomy and Neurobiology, University of Puerto Rico School of Medicine, San Juan, Puerto Rico 00936-5067
Correspondence should be addressed to Dr. Gregory J. Quirk, Department of Psychiatry, University of Puerto Rico School of Medicine, P.O. Box 365067, San Juan, Puerto Rico 00936-5067. Email: gjquirk{at}yahoo.com
During auditory fear conditioning, it is well established that lateral amygdala (LA) neurons potentiate their response to the tone conditioned stimulus, and that this potentiation is required for conditioned fear behavior. Conditioned tone responses in LA, however, last only a few hundred milliseconds and cannot be responsible for sustained fear responses to a tone lasting tens of seconds. Recent evidence from inactivation and stimulation studies suggests that the prelimbic (PL) prefrontal cortex is necessary for expression of learned fears, but the timing of PL tone responses and correlations with fear behavior have not been studied. Using multichannel unit recording techniques in behaving rats, we observed sustained conditioned tone responses in PL that were correlated with freezing behavior on a second-to-second basis during the presentation of a 30 s tone. PL tone responses were also correlated with conditioned freezing across different experimental phases (habituation, conditioning, extinction). Moreover, the persistence of PL responses after extinction training was associated with failure to express extinction memory. Together with previous inactivation findings, the present results suggest that PL transforms transient amygdala inputs to a sustained output that drives conditioned fear responses and gates the expression of extinction. Given the relatively long latency of conditioned responses we observed in PL (
100 ms after tone onset), we propose that PL integrates inputs from the amygdala, hippocampus, and other cortical sources to regulate the expression of fear memories.
Received Jan. 23, 2009;
revised May 21, 2009;
accepted May 22, 2009.
Correspondence should be addressed to Dr. Gregory J. Quirk, Department of Psychiatry, University of Puerto Rico School of Medicine, P.O. Box 365067, San Juan, Puerto Rico 00936-5067. Email: gjquirk{at}yahoo.com
Related articles in J. Neurosci.:
- Prelimbic Prefrontal Neurons Drive Fear Expression: A Clue for Extinction–Reconsolidation Interactions
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J. Neurosci. 2009 29: 13432-13434.
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D. Schiller and J. Johansen
Prelimbic Prefrontal Neurons Drive Fear Expression: A Clue for Extinction-Reconsolidation Interactions
J. Neurosci.,
October 28, 2009;
29(43):
13432 - 13434.
[Full Text]
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