Hippocampal function during behaviorally silent associative learning: Dissociation of memory storage and expression

In laboratory studies, the assessment of memory is typically associated with overt behavioral responses. Thus, it has been difficult to determine whether the enhancement of hippocampal sensory‐evoked potentials that often accompany memory formation are the neurophysiological manifestation of a memory “trace” or are a secondary product of the behavioral expression of the memory. We addressed this issue by examining changes in evoked hippocampal field potentials during sensory preconditioning, a form of behaviorally silent relational learning that requires an intact hippocampus for execution. Rats were exposed to presentations of a white noise (S1) that terminated with a tone (S2). These pairings of ostensibly “neutral” stimuli supported no change in the behavior elicited by the noise. However, if the tone was subsequently paired with mild footshock (US), suppression of ongoing licking behavior (indicative of fear) was elicited by the noise, indicating that the animal had associated the noise with tone (S1‐S2), and had represented the noise‐tone‐shock (S1‐S2‐US) relationship. Pre‐training neurotoxic lesions of the hippocampus had no effect on conditioned suppression to tone after tone‐shock (S2‐US) pairings, but disrupted the expression of continued suppression to noise (S1) after tone‐shock pairings. In a second experiment, sensory‐evoked field potentials in the dorsal hippocampus were recorded with extracellular electrodes. No changes in the hippocampal response evoked by white noise were observed after pairings of noise and tone, i.e., no evidence for a memory trace could be detected. In contrast, after tone was paired with footshock, two short‐latency negative potentials within the noise‐evoked field response increased in amplitude, a response often presumed to reflect a neurophysiological correlate of memory storage. In total, these results suggest that although the hippocampus critically contributes to the processing of a behaviorally silent associative memory, there may be no role for changes in the amplitude of hippocampal sensory‐evoked field potentials in storing representations of the relationships between sensory experiences. Hippocampus 2002;12:648–656. © 2002 Wiley‐Liss, Inc.