Trace Conditioning and the Hippocampus: The Importance of Contiguity

Abstract

Trace conditioning, a form of classical conditioning in which the presentation of the conditioned stimulus (CS) and the unconditioned stimulus (US) is separated in time by an interstimulus interval, requires an intact hippocampus. In contrast, classical conditioning procedures in which the CS and US are not separated by an interstimulus interval (i.e., delay conditioning procedures) typically do not (Solomon et al., 1986). However, why trace conditioning is dependent on the hippocampus is unknown. Several theories suggest that it is specifically the discontiguity between the CS and US in trace conditioning that critically engages the hippocampus. However, there are other explanations that do not depend on discontiguity. To determine whether the lack of contiguity renders trace conditioning hippocampal dependent, we designed a "contiguous trace conditioning" (CTC) paradigm in which CS-US contiguity is restored by representing the CS simultaneously with the US. Although rats with excitotoxic lesions of the hippocampus could not learn a standard trace fear-conditioning paradigm, lesioned rats trained on CTC showed significant conditioning, at levels similar to those with sham surgeries. Importantly, lesioned rats trained solely with simultaneous CS-US presentations did not demonstrate conditioning. Together, these data suggest that rats with hippocampal lesions can form a memory of a trace CS-US association when contiguity is restored. Therefore, the dependence of traditional trace paradigms on the hippocampus can be attributed to the absence of temporal contiguity.

Na+–Ca2+Exchanger (NCX3) Knock-Out Mice Display an Impairment in Hippocampal Long-Term Potentiation and Spatial Learning and Memory

“…D, Schematic representation of the temporal relationship between the CS and US for a single trial. The trace interval ensures that the task is sensitive to hippocampal function (Bangasser et al, 2006). E, Percentage of total time spent in the freeze status when NCX3 Ϫ/Ϫ and congenic NCX3 ϩ/ϩ mice were exposed to context or tone test.…”

“…Unlike delay tone conditioning, the acquisition of trace fear conditioning is sensitive to hippocampal lesions (McEchron et al, 1998;Desmedt et al, 2003;Bangasser et al, 2006) and to genetic modifications of the hippocampus (Huerta et al, 2000;D'Adamo et al, 2002). A fear-conditioning shock chamber (35 ϫ 23 cm, 19 cm height) containing a stainless steel rod floor (2.5 mm diameter, spaced 1 cm apart, Ugo Basile Inc.) and a high definition digital camera to monitor animal movements were used.…”

Mind the Gap: Olfactory Trace Conditioning in Honeybees

“…Thus, the mushroom body might equally be involved in resolving the ambiguous CS-US relationship in trace conditioning. Interestingly, the mammalian hippocampus is specifically needed for reversal learning (Berger and Orr, 1983), and it is thought to resolve the temporally ambiguous stimulus relationship in trace conditioning (Beylin et al, 2001;Bangasser et al, 2006).…”

Inhibition of learning and memory by general anesthetics

“…[42][43][44][45] Some types of fear conditioning, including the contextual and trace fear conditioning, also involve the hippocampus. [46][47][48][49][50][51] Unlike the hippocampus, the amygdala is necessary for the acquisition of fearful memories and their long-term storage and retrieval. 38,[52][53][54] In summary, explicit memory requires structures in the medial temporal lobe, such as the hippocampal formation and several cortical regions.…”