Abstract
The amygdala can modulate declarative memory. For example, previous research in rats and humans showed that brief electrical stimulation to the basolateral complex of the amygdala (BLA) prioritized specific objects to be consolidated into long term memory in the absence of emotional stimuli and without awareness of stimulation. The capacity of the BLA to influence memory depends on its substantial projections to many other brain regions, including the hippocampus. Nevertheless, how activation of the BLA influences ongoing neuronal activity in other regions is poorly understood. The current study used optogenetic stimulation of putative glutamatergic neurons in the BLA of freely exploring rats to determine whether brief activation of the BLA could increase in the hippocampus gamma oscillations for which the amplitude was modulated by the phase of theta oscillations, an oscillatory state previously reported to correlate with good memory. BLA neurons were stimulated in 1-s bouts with pulse frequencies that included the theta range (8 Hz), the gamma range (50 Hz), or a combination of both ranges (eight 50-Hz bursts). Local field potentials were recorded in the BLA and in the pyramidal layer of CA1 in the intermediate hippocampus. A key question was whether BLA stimulation at either theta or gamma frequencies could combine with ongoing hippocampal oscillations to result in theta-modulated gamma or whether BLA stimulation that included both theta and gamma frequencies would be necessary to increase theta–gamma comodulation in the hippocampus. All stimulation conditions elicited robust responses in BLA and CA1, but theta-modulated gamma oscillations increased in CA1 only when BLA stimulation included both theta and gamma frequencies. Longer bouts (5-s) of BLA stimulation resulted in hippocampal activity that evolved away from the initial oscillatory states and toward those characterized more by prominent low-frequency oscillations. The current results indicated that one mechanism by which the amygdala might influence declarative memory is by eliciting neuronal oscillatory states in the hippocampus that benefit memory.
Highlights
The basolateral complex of the amygdala (BLA) is a key modulatory region of hippocampus-dependent memory (McGaugh, 2002)
Inactivating the hippocampus via local infusion of muscimol blocked the object recognition memory improvement triggered by electrical stimulation of the BLA (Bass et al, 2014), whereas pharmacological manipulations of the BLA such as local infusion of adrenergic agonists led to increased markers of synaptic plasticity in the hippocampus (McIntyre et al, 2005; McReynolds et al, 2014a)
Recent studies using electrical stimulation to the BLA to enhance object recognition memory have used an electrical pulse frequency meant to simulate theta-modulated gamma oscillations. These results indicated that stimulating the BLA with a thetamodulated gamma pulse frequency was capable of improving memory performance, but the findings did not answer whether stimulating at theta or gamma frequencies alone would suffice to elicit in the hippocampus neuronal oscillations resembling those that correlate with good memory
Summary
The basolateral complex of the amygdala (BLA) is a key modulatory region of hippocampus-dependent memory (McGaugh, 2002). In one recent study with human participants, direct electrical stimulation targeting the BLA improved recognition memory for neutral object images despite participants reporting that they could not detect the stimulation (Inman et al, 2018) These experiments built on prior work in rodents demonstrating that the BLA mediated the influence of emotional arousal on memory performance in tasks such as inhibitory avoidance (McIntyre et al, 2002, 2005; McReynolds et al, 2010, 2014b; Holloway-Erickson et al, 2012; Huff et al, 2013). Many brain regions receive inputs from the BLA (Sah et al, 2003), but for modulation of hippocampusdependent memory, the current data suggest one key region influenced by the BLA is the hippocampus itself Understanding these mechanisms will help characterize how the brain prioritizes important memories (Manns and Bass, 2016)
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