Molecular and Physiological Plasticity in the Ventral Hippocampus Following Associative Fear Learning

Abstract

Pavlovian fear conditioning is useful for understanding how various brain regions support associative fear memory. The hippocampus plays an especially important role in fear learning. Evidence suggests disrupted dorsal and/or ventral hippocampal activity leads to pronounced fear memory deficits, and the dorsal hippocampus displays distinct plasticity changes following fear learning, including altered intrinsic excitability and immediate early gene expression. These mechanisms support fear memory consolidation. However, the molecular and physiological plasticity of the ventral hippocampus following various forms of fear learning remains poorly understood. The current experiments examine the nature of associative fear learning-related plastic changes in the ventral hippocampus by determining the effect of trace and context fear conditioning on immediate early gene expression and intrinsic excitability in this brain region. Our data indicate that 1) the ventral hippocampus displays selective increases of Arc and pCREB protein expression following context, but not trace, fear retrieval; 2) ventral hippocampal CA1 regular-spiking neurons display increased excitability following context fear conditioning, but not following trace fear conditioning; and 3) ventral hippocampal CA1 late-spiking neurons demonstrate heterogeneity of intrinsic plasticity following trace fear conditioning, such that neurons from good learners display increased excitability relative to neurons from poor learners. Together, these data highlight the unique contribution of the ventral hippocampus to context and trace fear conditioning, and suggest for the first time that distinct neuronal subpopulations within the ventral hippocampus can contribute to different types of associative fear memories.