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The hippocampus has long been implicated in memory processes, specifically contextual memory of conditioned fear (Kim & Fanselow, 1992; Phillips & LeDoux, 1992). Recent research by Wilson, Brooks and Bouton (1995) demonstrated that radiofrequency lesions of the fornix, the major output pathway of the hippocampus, disrupted reinstatement, but not renewal. Reinstatement is the recovery of responding to an extinguished conditioned stimulus (CS) following independent presentations of the unconditioned stimulus (US). Renewal is the recovery of responding when the CS is presented in the context in which it was conditioned following extinction in a different context. We specifically examined the role of the hippocampus in mediating these two effects of context during extinction.

Rats received either lesions with 6 infusions (3 per hemisphere) of an ibotenic acid (10 mg/ml) and NMDA (10 mg/ml) cocktail into the hippocampus or sham surgery. Following recovery, food deprivation and baseline lever training for food, animals received conditioned emotional responding (CER) training. In Experiment 1animals were tested for reinstatement. In Experiments 2 & 3 animals were tested for renewal in a standard, or condensed version. Results indicate that neurotoxic lesions of the hippocampus disrupt reinstatement, which depends on context-US associations, but not renewal, which does not. In addition, the effect of the lesions on reinstatement does not seem to depend on the recency of the context-US learning relative to the renewal paradigm.


Recent evidence suggests that the hippocampal formation is important for learning about contextual stimuli (e.g., Holland & Bouton, 1999). However, evidence also suggests that not all types of learning about the context are hippocampal-dependent (Good & Honey, 1991; McDonald, Murphy, Guarraci, Gortler, White & Baker, 1997). The overall pattern is thus not entirely consistent with the idea that the hippocampus is necessary to form a coherent representation of the context that might be required for all forms of context learning (cf. Fanselow, DeCola, & Young, 1993).

The present experiments further examined the role of hippocampus in context learning by investigating its role in the contextual control of performance following fear extinction. Extinction is the behavioral phenomenon in which exposure to the conditioned stimulus (CS) on its own eliminates performance created after CS-unconditioned stimulus (US) pairings. The present experiments examined two examples of contextual control which suggest that extinction performance depends on the current context (e.g., see Bouton, 1991, 1993 for reviews). Although both are clearly context effects, behavioral research in this laboratory has shown that the two effects are controlled by different kinds of context learning.

The first effect, reinstatement, occurs when exposure to the US alone after extinction causes a recovery of responding to the CS when it is tested later (e.g., Bouton & Bolles, 1979b; Rescorla & Heth, 1975). The second effect of context we examined here is renewal. In this effect, conditioning that occurs because of CS-US pairings in one context (Context A) is then extinguished in a second context (Context B). When the CS is presented again in the conditioning context (Context A), “renewed” responding is observed (e.g., Bouton & Bolles, 1979a; Bouton & King, 1983).

Wilson, Brooks & Bouton (1995) found that fornix lesions abolished reinstatement but left the renewal effect relatively intact. The fact that the fornix lesion specifically abolished reinstatement suggests that the hippocampus is necessary for the learning or expression of context-footshock associations (e.g., Kim & Fanselow, 1992; Phillips & LeDoux, 1992). In contrast, the lesion spares the occasion-setting like function of context represented by the renewal effect. The purpose of the present experiments was to pursue the dissociation further.

Common Methods


  • Neurotoxic lesions of the hippocampus

    • 10 mg/ml Ibotenic Acid + 10 mg/ml NMDA cocktail


  • All animals 80% of free feeding weight

  • 6 days of VI-90 training in alternating contexts


  • Animals were exposed to the context opposite of training on alternating days in order to control for exposure to the two contexts



Sham Same A:L+/B:- A:L-/B:- A:+ A:L-Sham Diff A:L+/B:- A:L-/B:- B:+ A:L- Hipp Same A:L+/B:- A:L-/B:- A:+ A:L- Hipp Diff A:L+/B:- A:L-/B:- B:+ A:L-

Days: 1-4 5-12 13 14

Note: A & B = Contexts, L = Light, + = Footshock, - = No Footshock

Reinstatement:Acquisition and Extinction

Suppression Ratio

2-Trial Blocks

4-Trial Blocks

Experiment 2RENEWAL


Sham A A:L+/B:- A:L-/B:- A:L- Sham B A:L+/B:- B:L-/B:- A:L- Hipp A A:L+/B:- A:L-/B:- A:L- Hipp B A:L+/B:- B:L-/B:- A:L-

Days: 1-4 5-12 13

Renewal:Acquisition and Extinction

Suppression Ratio

2-Trial Blocks

4-Trial Blocks



Sham A A:L+ A:L- A:L- Sham B A:L+ B:L- A:L- Hipp A A:L+ A:L- A:L- Hipp B A:L+ B:L- A:L-

Days: 1 2 3

Short Renewal:Acquisition and Extinction

Suppression Ratio

2-Trial Blocks

4-Trial Blocks

Short Renewal

Suppression Ratio



  • The hippocampus is not required for all forms of context learning

  • Hippocampal lesions disrupt reinstatement but not renewal

  • The disruption is not due to the recency of the context learning in reinstatement

  • The hippocampus may be required for learning direct context-shock associations