Context fear learning in the absence of the hippocampus

Abstract

Lesions of the rodent hippocampus invariably abolish context fear memories formed in the recent past but do not always prevent new learning. To better understand this discrepancy, we thoroughly examined the acquisition of context fear in rats with pretraining excitotoxic lesions of the dorsal hippocampus. In the first experiment, animals received a shock immediately after placement in the context or after variable delays. Immediate shock produced no context fear learning in lesioned rats or controls. In contrast, delayed shock produced robust context fear learning in both groups. The absence of fear with immediate shock occurs because animals need time to form a representation of the context before shock is presented. The fact that it occurs in both sham and lesioned rats suggests that they learn about the context in a similar manner. However, despite learning about the context in the delay condition, lesioned rats did not acquire as much fear as controls. The second experiment showed that this lesion-induced deficit could be overcome by increasing the number of conditioning trials. Lesioned animals learned normally after multiple shocks, regardless of freezing level or trial spacing. The last experiment showed that animals with complete hippocampus lesions could also learn about the context, although the same lesions produced devastating retrograde amnesia. These results demonstrate that alternative systems can acquire context fear but do so less efficiently than the hippocampus.

Figure 1.

Photomicrographs showing thionin-stained coronal brain sections after excitotoxic lesions of the dorsal hippocampus. From top to bottom, the sections are −0.80, −1.60, −2.60, −3.60, −4.60, and −6.0 mm posterior to bregma.

Figure 2.

Mean ± SEM percentage freezing during the context test for sham and DH-lesioned animals. A, Freezing levels for animals that received an immediate or delayed shock. B, Freezing levels for animals that received shock 12, 24, 48, 192, or 340 s after placement in the context during training. *p < 0.05, significant group difference.

Figure 3.

Mean ± SEM percentage freezing during the context test for sham and DH-lesioned animals. Separate groups of animals received one or three shocks during a 48 or 340 s training session. *p < 0.05, significant group difference.

Figure 4.

Mean ± SEM percentage freezing during each minute of the context test for sham and DH-lesioned animals. A, Freezing time course for animals receiving a single shock during training. B, Freezing time course for animals receiving three shocks during training.

Figure 5.

Mean ± SEM velocity (in centimeters per second) for sham and DH-lesioned animals during the 2 s shock and an equivalent baseline period. A, Velocity for animals receiving a single shock. B, Velocity for animals receiving three shocks.

Figure 6.

Photomicrographs showing thionin-stained coronal brain sections after excitotoxic lesions of the dorsal and ventral hippocampus (left) or sham surgery (right). From top to bottom, the sections are −0.30, −1.80, −3.0, −4.0, −4.50, and −4.60 mm posterior to bregma.

Figure 7.

Mean ± SEM percentage freezing during the context test after posttraining (Retro) or pretraining (Antero) lesions of the hippocampus. Lesions made 1 d after intense training produced robust retrograde amnesia for context fear. Anterograde amnesia was not observed after moderate retraining. *p < 0.05, significant group difference.