Odor Fear Conditioning Modifies Piriform Cortex Local Field Potentials Both during Conditioning and during Post-Conditioning Sleep

BACKGROUND: Sleep plays an active role in memory consolidation. Sleep structure (REM/Slow wave activity [SWS]) can be modified after learning, and in some cortical circuits, sleep is associated with replay of the learned experience. While the majority of this work has focused on neocortical and hippocampal circuits, the olfactory system may offer unique advantages as a model system for exploring sleep and memory, given the short, non-thalamic pathway from nose to primary olfactory (piriform cortex), and rapid cortex-dependent odor learning. METHODOLOGY/PRINCIPAL FINDINGS: We examined piriform cortical odor responses using local field potentials (LFPs) from freely behaving Long-Evans hooded rats over the sleep-wake cycle, and the neuronal modifications that occurred within the piriform cortex both during and after odor-fear conditioning. We also recorded LFPs from naïve animals to characterize sleep activity in the piriform cortex and to analyze transient odor-evoked cortical responses during different sleep stages. Naïve rats in their home cages spent 40% of their time in SWS, during which the piriform cortex was significantly hypo-responsive to odor stimulation compared to awake and REM sleep states. Rats trained in the paired odor-shock conditioning paradigm developed enhanced conditioned odor evoked gamma frequency activity in the piriform cortex over the course of training compared to pseudo-conditioned rats. Furthermore, conditioned rats spent significantly more time in SWS immediately post-training both compared to pre-training days and compared to pseudo-conditioned rats. The increase in SWS immediately after training significantly correlated with the duration of odor-evoked freezing the following day. CONCLUSIONS/SIGNIFICANCE: The rat piriform cortex is hypo-responsive to odors during SWS which accounts for nearly 40% of each 24 hour period. The duration of slow-wave activity in the piriform cortex is enhanced immediately post-conditioning, and this increase is significantly correlated with subsequent memory performance. Together, these results suggest the piriform cortex may go offline during SWS to facilitate consolidation of learned odors with reduced external interference

The basolateral amygdala is necessary for the encoding and the expression of odor memory

Conditioned odor avoidance (COA) results from the association between a novel odor and a delayed visceral illness. The present experiments investigated the role of the basolateral amygdala (BLA) in acquisition and retrieval of COA memory. To address this, we used the GABA(A) agonist muscimol to temporarily inactivate the BLA during COA acquisition or expression. BLA inactivation before odor-malaise pairing greatly impaired COA tested 3 d later. In contrast, muscimol microinfusion between odor and malaise spared retention. Moreover, inactivation of the BLA before pre-exposure to the odor prevented latent inhibition of COA. This suggests that neural activity in the BLA is essential for the formation of odor representation. BLA inactivation before the retrieval test also blocked COA memory expression when performed either 3 d (recent memory) or 28 d (remote memory) after acquisition. This effect was transitory as muscimol-treated animals were not different from controls during the subsequent extinction tests. Moreover, muscimol infusion in the BLA neither affected olfactory perception nor avoidance behavior, and it did not induce a state-dependent learning. Altogether, these findings suggest that neural activity in the BLA is required for the encoding and the retrieval of odor memory. Moreover, the BLA seems to play a permanent role in the expression of COA

The basolateral amygdala is necessary for the encoding and the expression of odor memory

International audienceConditioned odor avoidance (COA) results from the association between a novel odor and a delayed visceral illness. The present experiments investigated the role of the basolateral amygdala (BLA) in acquisition and retrieval of COA memory. To address this, we used the GABA(A) agonist muscimol to temporarily inactivate the BLA during COA acquisition or expression. BLA inactivation before odor-malaise pairing greatly impaired COA tested 3 d later. In contrast, muscimol microinfusion between odor and malaise spared retention. Moreover, inactivation of the BLA before pre-exposure to the odor prevented latent inhibition of COA. This suggests that neural activity in the BLA is essential for the formation of odor representation. BLA inactivation before the retrieval test also blocked COA memory expression when performed either 3 d (recent memory) or 28 d (remote memory) after acquisition. This effect was transitory as muscimol-treated animals were not different from controls during the subsequent extinction tests. Moreover, muscimol infusion in the BLA neither affected olfactory perception nor avoidance behavior, and it did not induce a state-dependent learning. Altogether, these findings suggest that neural activity in the BLA is required for the encoding and the retrieval of odor memory. Moreover, the BLA seems to play a permanent role in the expression of COA

Effets de l'odorisation des mamelles maternelles sur les apprentissages et comportements alimentaires olfactifs à l'âge adulte

National audienc

Dissociation of the role of infralimbic cortex in learning and consolidation of extinction of recent and remote aversion memory

Medial prefrontal circuits have been reported to undergo a major reorganization over time and gradually take a more important role for remote emotional memories such as contextual fear memory or food aversion memory. The medial prefrontal cortex, and specifically its ventral subregion, the infralimbic cortex (IL), was also reported to be critical for recent memory extinction of contextual fear conditioning and conditioned odor aversion. However, its exact role in the extinction of remotely acquired information is still not clear. Using postretrieval blockade of protein synthesis or inactivation of the IL, we showed that the IL is similarly required for extinction consolidation of recent and remote fear memory. However, in odor aversion memory, the IL was only involved in extinction consolidation of recent, but not remote, memory. In contrast, only remote retrieval of aversion memory induced c-Fos activation in the IL and preretrieval inactivation of the IL with lidocaine impaired subsequent extinction of remote but not recent memory, indicating IL is necessary for extinction learning of remote aversion memory. In contrast to the effects in odor aversion, our data show that the involvement of the IL in the consolidation of fear extinction does not depend on the memory age. More importantly, our data indicate that the IL is implicated in the extinction of fear and nonfear-based associations and suggest dissociation in the engagement of the IL in the learning and consolidation of food aversion extinction over time