Fornix lesions can facilitate acquisition of the transverse patterning task: a challenge for "configural" theories of hippocampal function

Abstract

Configural theories of hippocampal function predict that hippocampal dysfunction should impair acquisition of the transverse patterning task, which involves the concurrent solution of three discrimination problems: A+ versus B-; B+ versus C-; and C+ versus A-. The present study tested this prediction in rats using computer-graphic stimuli presented on a touchscreen. Experiment 1 assessed the effects of fornix lesions when the three problems were introduced sequentially (phase 1: A+ vs B-; phase 2: A+ vs B-, B+ vs C-; phase 3: A+ vs B-, B+ vs C-, C+ vs A-). Fornix lesions significantly facilitated acquisition of the complete transverse patterning task (phase 3) but had no effect on the number of sessions or errors required to attain criterion during phase 1 or phase 2. In experiment 2, in which all three problems were presented concurrently from the outset of training, fornix-lesioned animals outperformed control animals during the seventh block of acquisition trials and were not impaired during any stage of acquisition. Importantly, these same animals were significantly impaired on two allocentric spatial tasks: T-maze alternation (experiments 1 and 2) and the Morris Swim Task (experiment 1). These results contradict the predictions of configural theories of hippocampal function and cast doubt on the popular notion that spatial learning is a special case of configural learning.

Fig. 1.

The touchscreen apparatus. A, Video display unit; B, Perspex “mask” with response windows and “shelf”; C, fan; D, pressure-sensitive floor panel; E, magazine;F, pellet dispenser (from Bussey et al., 1994).

Fig. 2.

Computer-graphic stimuli used in the transverse patterning task. The figure provides the outline of the stimuli, which were drawn against a black background in blue (A), green (B), and white (C).

Fig. 3.

Coronal sections illustrating the extent of the largest (gray) and smallest (black) lesions of the fornix in groupFNX1 (experiment 1) at −0.92 cm (section22) and −1.30 cm (section 23) from Bregma according to the atlas of Paxinos and Watson (1997).

Fig. 4.

Acquisition curves for animals of theFNX1 and Sham1 groups on the transverse patterning task (phase 3 of experiment 1: sequential training). Error bars indicate +/−SEM.

Fig. 5.

Performance levels of the FNX1,Sham1, FNX2, and Sham2groups on each of the three problems of the full transverse patterning problem in experiments 1 and 2. Data are mean percent correct scores on the final four-session block of acquisition for each problem.Asterisks indicate significant differences; ***p < 0.001; **p = 0.01; *p < 0.05.

Fig. 6.

Percent correct scores of animals of theFNX1 and Sham1 groups on the first sessions of phase 2 (left) and phase 3 (right) in experiment 1. Animals of theFNX1 group obtained significantly lower scores than did control animals during the first session of problem 2 in phase 2, suggesting differential transfer of learning from phase 1. Note also the pattern of results during phase 3, in which all animals solve one problem very well, another at approximately chance level performance, and the third at well below chance, a pattern that may indicate an attempt at an “elemental” solution. Error bars indicate +/−SEM.Asterisk denotes a significant difference fromSham1 animals at p < 0.05.

Fig. 7.

Mean percent correct scores of animals of theFNX1, Sham1, FNX2, andSham2 groups on T-maze alternation in experiments 1 and 2. Error bars indicate +/−SEM.

Fig. 8.

Performance of animals of the FNX1and Sham1 groups on the Morris Swim Task. The top panel shows mean escape latencies, and the bottom panel shows the percentage of time spent swimming within 15 cm from the walls of the pool.

Fig. 9.

Coronal sections illustrating the extent of the largest (gray) and smallest (white) lesions of the fornix in group FNX 2 (experiment 2) at −0.92 cm (section 22) and −1.30 cm (section 23) from Bregma according to the atlas of Paxinos and Watson (1997).

Fig. 10.

Acquisition curves for animals of theFNX2 and Sham2 groups on the transverse patterning task (experiment 2: concurrent training). Error bars indicate +/−SEM.