The Journal of Neuroscience, January 1, 1998, 18(1):480-487
Differential Modulation of Changes in Hippocampal-Septal
Synaptic Excitability by the Amygdala as a Function of Either Elemental
or Contextual Fear Conditioning in Mice
Aline
Desmedt,
René
Garcia, and
Robert
Jaffard
Laboratoire de Neurosciences Comportementales et Cognitives, Centre
National de la Recherche Scientifique Unité de Recherche
Associée 339, Université de Bordeaux I, 33405 Talence,
France
Recent data obtained using a classic fear conditioning paradigm
showed a dissociation between the retention of associations relative to contextual information (dependent on the hippocampal formation) and the retention of elemental associations (dependent on
the amygdala). Furthermore, it was reported that conditioned emotional
responses (CERs) could be dissociated from the recollection of the
learning experience (declarative memory) in humans and from
modifications of the hippocampal-septal excitability in animals. Our
aim was to determine whether these two systems ("behavioral expression" system and "factual memory" system) interact by
examining the consequences of amygdalar lesions (1) on the
modifications of hippocampal-septal excitability and (2) on the
behavioral expression of fear (freezing) resulting from an aversive
conditioning during reexposure to conditional stimuli (CSs). During
conditioning, to modulate the predictive nature of the context and of a
discrete stimulus (tone) on the unconditional stimulus (US) occurrence, the phasic discrete CS was paired with the US or randomly distributed with regard to the US. After the lesion, the CER was dramatically reduced during reexposure to the CSs, whatever the type of acquisition. However, the changes in hippocampal-septal excitability persisted but
were altered. For controls, a decrease in septal excitability was
observed during reexposure to the conditioning context only for the
"unpaired group" (predictive context case). Conversely, among
lesioned subjects this decrease was observed in the "paired group"
(predictive discrete CS case), whereas this decrease was significantly
reduced in the unpaired group with respect to the matched control
group. The amplitude and the direction of these modifications
suggest a differential modulation of hippocampal-septal excitability by the amygdala to amplify the contribution of the more
predictive association signaling the occurrence of the aversive event.
Key words:
amygdala central nucleus; lateral septum; hippocampal-septal excitability; elemental versus contextual
conditioning; fear conditioning; mice
Copyright © 1998 Society for Neuroscience 0270-6474/98/181480-08$05.00/0