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

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.