Synaptic plasticity in the basolateral amygdala induced by hippocampal formation stimulation in vivo

Abstract

Several studies suggest that axonal projections from the hippocampal formation (HF) to the basolateral amygdala (BLA) play a role in Pavlovian fear conditioning to contextual conditional stimuli. We have used electrophysiological techniques to characterize neuronal transmission in these projections in urethane-anesthetized rats. Single-pulse electrical stimulation of the ventral angular bundle (VAB), which carries projections from the HF to the BLA, reliably evoked a biphasic extracellular field potential in the BLA that consisted of an early, negative and a late, positive component. The negative component of the field potential occurred at a short latency (3-8 msec), was both temporally and spatially correlated with VAB-evoked multiple-unit discharges in the BLA, and exhibited properties typical of a monosynaptic response. Infusion of lidocaine or glutamate receptor antagonists into the BLA attenuated VAB-evoked field potentials, indicating that they are generated by local synaptic glutamatergic transmission. Both paired-pulse stimulation and brief trains of high-frequency stimulation (HFS) induced a short-lasting facilitation of BLA field potentials, whereas longer and more numerous trains of HFS produced an enduring, NMDA receptor-dependent long-term potentiation (LTP) of the potentials. The induction of LTP was accompanied by a decrease in paired-pulse facilitation (PPF), suggesting a presynpatic modification underlying its expression. Electrolytic lesions placed in regions of the HF that project to the BLA or excitotoxic lesions placed in the BLA eliminated Pavlovian fear conditioning to a contextual conditional stimulus. The critical role of both structures in context conditioning implicates plasticity at HF-BLA synapses in this form of learning.