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

Abstract

ABSTRACT: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 sensoryevoked 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 noisetone-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.

Role of the basolateral amygdala and NMDA receptors in higher-order conditioned fear

“…Moreover, Nicholson and Freeman (2000) showed that rats with lesions of the perirhinal cortex (PRh), a region of the parahippocampus, that are exposed to pairings of a light and tone and then to pairings of the tone with periorbital shock show protective refl exes to the tone but not to the light. These results indicate that the parahippocampal region is involved in forming an association between two neutral stimuli and is consistent with the suggestion that the medial temporal lobe is necessary for associative formation between non-reinforced stimuli (Eichenbaum et al, 1992;Talk et al , 2002 ). Taken together with the results of Parkes and Westbrook (2010), these results also suggest that NMDAr activation in the parahippocampal region could mediate the acquisition and the extinction of an association between two neutral stimuli.…”

“…Early studies identifi ed an involvement of the hippocampus in learning associations between neutral stimuli (Port and Patterson , 1984 ;Port et al , 1987 ; see also Talk et al , 2002 ). However, it has been reported that more selective lesions that leave parahippocampal regions intact do not impair sensory preconditioning (Ward -Robinson et al, 2001 ).…”

A Computational Model of the Functional Role of the Ventral-Striatal D2 Receptor in the Expression of Previously Acquired Behaviors

“…Although the types of representation used by animals are many and varied (Balleine, Garner, Gonzalez, & Dickinson, 1995;Berridge & Robinson, 1998;Cardinal, Parkinson, Hall, & Everitt, 2002;Dickinson, 1980), the evidence that animals internally represent action-outcome relationships (among others) is compelling (Dickinson, 1987;Dickinson, Nicholas, & Adams, 1983). For example, Dickinson (1980) reviews the sensory preconditioning paradigm (Nader & LeDoux, 1999;Rizley & Rescorla, 1972;Talk, Gandhi, & Matzel, 2002;Young, Ahier, Upton, Joseph, & Gray, 1998). During stage 1, a tone is paired with food.…”

Latent Learning and Deferred Imitation at 3 Months

“…Because the association that individuals learn during sensory preconditioning is latent or covert at the time it is formed, it has been characterized as "behaviorally silent" learning (Domjan, 2003;Talk, Gandhi, & Matzel, 2002). We now report that 3-month-olds who were tested in a sensory preconditioning paradigm formed a latent association between two objects they merely saw together (Experiment 1 a) and formed a second association between one of the objects and a sequence of target actions they saw an adult perform on it (Experiment lb).…”