Disconnection analysis of CA3 and DG in mediating encoding but not retrieval in a spatial maze learning task

Abstract

The dentate gyrus (DG) subregion of the hippocampus has been shown to be involved in encoding but not retrieval in a spatial maze task (modified Hebb-Williams maze). The first experiment in this study examined whether a lesion to the CA3 would contribute to a similar encoding deficit. A DG group was included in order to replicate previous results. Relative to controls, animals receiving CA3 lesions were impaired in encoding, not retrieval, on the modified Hebb-Williams maze--similar to a group that received DG lesions. This suggests the possibility that CA3 and DG are working together to mediate encoding processes. The second experiment in this study was designed to test the interaction between CA3 and DG using a disconnection paradigm. Animals with contralateral lesions (CA3 lesioned in one hemisphere, DG lesioned in the other hemisphere) showed a significant disruption effect on encoding, but not retrieval, when compared with animals with ipsilateral lesions (CA3 and DG lesioned in the same hemisphere, leaving the other hemisphere intact). This suggests an interaction between CA3 and DG in supporting encoding but not retrieval processes in a spatial maze learning task.

Figure 1.

Representative photomicrographs (12×) of lesions to hippocampal subregions. (A) Dentate gyrus colchicine-induced lesion. (B) CA3 ibotenic acid lesion. (C) Contralateral lesion of dentate gyrus (left) and CA3 (right). (D) Ipsilateral lesion of dentate gyrus and CA3 resulting in full unilateral hippocampal ablation. See Results for quantitative analysis.

Figure 2.

Mean number of errors per trial were grouped in five-trial blocks across a total of 3 d of acquisition in the Hebb-Williams maze for the control, CA3, and dentate gyrus (DG) groups. The CA3 lesions group made more errors than DG or control groups as determined by a Tukey HSD paired comparison (P < 0.05).

Figure 3.

(A) Mean encoding index in the Hebb-Williams maze for the control, CA3, and dentate gyrus (DG) groups. (B) Mean retrieval index in the Hebb-Williams maze for the control, CA3, and dentate gyrus (DG) groups. The results show that CA3 and DG groups disrupt encoding but have no deleterious effects on retrieval. Asterisks (*) correspond to significant differences from controls (P < 0.01) as determined by Tukey HSD paired-comparison test.

Figure 4.

Mean number of errors per trial were grouped in five-trial blocks across a total of 3 d of acquisition in the Hebb-Williams maze for the contralateral and ipsilateral lesion groups. The results show that the contralateral, but not ipsilateral, treatment disrupted encoding, but neither group had any deleterious effects on retrieval.

Figure 5.

(A) Mean encoding index in the Hebb-Williams maze for the control, contralateral, and ipsilateral lesions groups. (B) Mean retrieval index in the Hebb-Williams maze for the control, contralateral, and ipsilateral lesions groups. Asterisks (*) correspond to significant differences from controls (P < 0.01) as determined by the Tukey HSD paired-comparison test.