Theta activity in neurons and networks of the amygdala related to long-term fear memory

Abstract

With a combined in vitro/in vivo electrophysiological and behavioral approach, we have correlated conditioned fear behavior to electrophysiological activities in the lateral amygdala and the hippocampal formation in rodents. Data indicate that projection neurons in the lateral amygdala display a continuum of spike patterns including accommodating patterns, regular firing, and oscillatory activity at theta frequencies. The firing pattern is controlled to an important part by the intracellular cAMP system, in that an increase in intracellular cAMP concentration facilitates regular firing and theta oscillations. Oscillatory electrical activity, in turn, provides an important cellular element of synchronized theta activity at 4-8 Hz (indicating atropine-sensitive type 2 theta) occurring in amygdalo-hippocampal pathways during conditioned fear responses. This type of rhythmic network activity is associated with the retrieval of long-term fear memory following cued and contextual fear conditioning, but is not related to the expression of fear behavior per se or to short-term fear memory. Synchronization at theta frequencies is suggested to represent activity in amygdalo-hippocampal pathways associated with system consolidation of fear memory, which is supported by the cholinergic system.