Synaptic Plasticity, Engrams, and Network Oscillations in Amygdala Circuits for Storage and Retrieval of Emotional Memories

Abstract

The neuronal circuits of the basolateral amygdala (BLA) are crucial for acquisition, consolidation, retrieval, and extinction of associative emotional memories. Synaptic plasticity in BLA neurons is essential for associative emotional learning and is a candidate mechanism through which subsets of BLA neurons (commonly termed "engram") are recruited during learning and reactivated during memory retrieval. In parallel, synchronous oscillations in the theta and gamma bands between the BLA and interconnected structures have been shown to occur during consolidation and retrieval of emotional memories. Understanding how these cellular and network phenomena interact is vital to decipher the roles of emotional memory formation and storage in the healthy and pathological brain. Here, we review data on synaptic plasticity, engrams, and network oscillations in the rodent BLA. We explore mechanisms through which synaptic plasticity, engrams, and long-range synchrony might be interconnected.

A Distinctive Pattern of Hippocampal-Prefrontal Cortical Network Activity during Stress Predicts Learned Resistance

“…We found that resistant and helpless individuals share electrophysiological markers of stress, but only resistant animals present the neural signature of controllability, in line with Maier and Seligman (2016). Considering that theta oscillations regulate synaptic plasticity and learning (Bocchio et al, 2017;Buzsáki, 2002;Hasselmo and Stern, 2014), theta activity impairments in helplessness could also mean that this syndrome stems from learning deficits rather than a learned response.…”

“…Mounting evidence indicates that theta oscillations have a role in the processing of aversive information (Bocchio et al, 2017;Çalışkan and Stork, 2019;Gray and McNaughton, 2000;Likhtik and Gordon, 2014). Many reports describe increased theta power and synchrony during different stressors, including exposure to distant predators, aggressive conspecifics, anxiogenic environments, and conditioned fear (Adhikari et al, 2010;Hultman et al, 2018;Lesting et al, 2011;Mikulovic et al, 2018;Sainsbury et al, 1987;Seidenbecher et al, 2003).…”

Cholecystokinin immunoreactive neurons in the basolateral amygdala of the rhesus monkey (Macaca mulatta)

“…Interneuronal networks in the cortex and BNC are important for their contribution to rhythmic oscillations in these regions (Benardo, 1997;Bienvenu et al, 2012;Buzsáki & Chrobak, 1995;Whittington, Traub, & Jefferys, 1995). These interneuronal network rhythms, as well as intrinsic oscillations in BNC PNs (Pape, Paré, & Driesang, 1998), are critical for synaptic plasticity associated with the formation and retrieval of emotional memories (Bocchio, Nabavi, & Capogna, 2017;Pape & Paré, 2010;Paré, Collins, & Pelletier, 2002).…”

Garth J. Thomas, Physiological Psychologist: An Appraisal of His Contributions to Memory Research

“…With regard to associative emotional learning, it appears that neurons of the basolateral amygdala are recruited during learning, and become reactivated during memory retrieval [60]. …”