Amygdala-mediated enhancement of memory for specific events depends on the hippocampus

Abstract

Emotional events are often remembered better than neutral events, a type of memory prioritization by affective salience that depends on the amygdala. Studies with rats have indicated that direct activation of the basolateral complex of the amygdala (BLA) can enhance memory for neutral events, and if the activation is brief and temporally targeted, can do so in a way that benefits memories for specific events. The essential targets of BLA activation in the case of event-specific memory enhancement were unknown, but the hippocampus was known to receive direct projections from the BLA and to support memory for events. In the present study, rats received counterbalanced infusions of either muscimol, a GABAA receptor agonist, or saline into the hippocampus prior to performing a novel object recognition memory task during which initial encounters with some of the objects were immediately followed by brief electrical stimulation to the BLA. When memory was tested 1day later in the saline condition, rats remembered these objects well but showed no memory for objects for which the initial encounter had not been followed by BLA stimulation. In contrast, no benefit to memory of BLA stimulation was observed in the muscimol condition. The results indicated that brief activation of the BLA can prioritize memories for events by enhancing memory for some object encounters but not others and that this benefit to memory depends on interactions between the amygdala and the hippocampus.

Keywords: Basolateral amygdala; Electrical stimulation; Fluorophore-conjugated muscimol; Hippocampus; Memory enhancement; Object recognition memory.

Copyright © 2013 Elsevier Inc. All rights reserved.

Figures

Figure 1

Schematic of infusion and object recognition memory procedures. Rats were infused with fluorophore-conjugated muscimol (FCM) or control vehicle (phosphate-buffered saline; PBS) 30 minutes prior to testing. In each trial of the Study Phase, rats encountered 3 novel objects such that there was one object from each group of objects (Stimulation objects denoted by an “S”, No Stimulation objects denoted by an “O”, and New objects denoted by an “N”). All objects were presented on individual laps to better isolate the influence of electrical stimulation to the amygdala. Electrical stimulation (denoted by a star) was delivered immediately following encounters with Stimulation objects. Memory for objects from half of the trials was tested during the Immediate Test, and memory for objects from the other half was tested during the 1-Day Test. Corresponding test trials contained duplicates of Stimulation and No Stimulation objects, but New objects were replaced by additional novel objects. All 3 objects were presented together on one lap. No stimulation was delivered during either test phase.

Figure 2

Example photomicrographs of histology. A. Stimulating electrode localization in the BLA (dashed outline) as shown on tissue stained for acetylcholinesterase. The tips of all electrodes for all rats included in the analyses were contained in the BLA (lateral nucleus, L; basal nucleus, B; accessory basal nucleus, AB). B. Fluorescent image of an infusion of FCM into the hippocampus. Infusions of FCM for all rats included in the analyses appeared to be contained within the hippocampus. The tips of all injection cannulae were localized near CA2 (between CA1 and CA3 fields) in the transverse axis and at an intermediate region of the septal-temporal axis of the hippocampus.

Figure 3

Performance on recognition memory tests following infusions of FCM or control vehicle (PBS) represented as a discrimination index. Following infusions of PBS into the hippocampus, rats demonstrated memory for both groups of repeated objects during the Immediate Test but showed memory for only Stimulation objects on the 1-Day Test. Following infusions of FCM into the hippocampus, rats did not demonstrate memory for objects in either test phase. The dashed line indicates chance performance. Error bars show SEM. * = p