Fear conditioning modulates the intrinsic excitability of ventral hippocampal CA1 neurons in male rats.

Abstract

The hippocampus has a known role in learning and memory, with the ventral subregion supporting many learning tasks involving affective responding, including fear conditioning. Altered neuronal intrinsic excitability reflects experience-dependent plasticity that supports learning-related behavioral changes. Such changes have previously been observed in the dorsal hippocampus following fear conditioning, but little work has examined the effect of fear conditioning on ventral hippocampal intrinsic plasticity. The present study tested the hypothesis that acquisition of trace and context fear conditioning alters intrinsic excitability of specific classes of ventral hippocampal CA1 neurons in male rats. We observed distinct changes in excitability that were specific to cell type and learning paradigm. Specifically, regular-spiking ventral hippocampal CA1 neurons demonstrated increased excitability following context fear conditioning, and these changes were correlated with context fear retrieval. In contrast, trace fear conditioning resulted in increased excitability of ventral hippocampal CA1 late-spiking neurons from good learners relative to poor learners. Together, these data demonstrate ventral hippocampal CA1 neuronal excitability is finely tuned to support fear memory in a learning- and firing type-specific manner.NEW & NOTEWORTHY This study is the first to characterize ventral hippocampal CA1 physiological firing types in associative fear learning. Distinct intrinsic excitability changes among these populations suggest they contribute uniquely to trace and context fear memory. These findings have important implications for anxiety disorders that depend on the ventral hippocampus and pave the way for future studies to examine how these populations might coordinate with the larger ventral hippocampal network in forming fear associations.