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.

The aging hippocampus: A multi-level analysis in the rat

“…Also, Rondi-Reig et al (2001) tested mice lacking CA1 NMDA receptors on the transverse patterning problem that required simultaneous acquisition of three odor discriminations comprising the transverse patterning problem contrasted with concurrent learning of three simple odor discriminations. They found that CA1 NMDA receptor knock-out mice were impaired in solving the transverse patterning odor discrimination compared with normal performance on the non-overlapping (elemental) concurrent odor discriminations (but see Bussey et al, 1998). To the best of our knowledge, prior to the present work, the transverse patterning task has not been previously employed in the studies of aged animals.…”

“…There have been several reports of anterograde amnesia for the transverse patterning problem after the damage to the hippocampus (Alvarado & Rudy, 1995a,b;Dusek & Eichenbaum, 1998; but see Bussey et al, 1998). For example, Alvarado and Rudy (1995a) found that rats with damage to the hippocampus could not solve the transverse patterning problem, but they readily learned to solve a control set of three elemental discrimination problems.…”

CA1-specific N -methyl- d -aspartate receptor knockout mice are deficient in solving a nonspatial transverse patterning task

“…Dusek and Eichenbaum found that rats with hippocampal damage succeeded in the initial training stages but failed in performing the concurrent random presentations. Bussey et al (21) trained animals in a protocol similar to that of Alvarado and Rudy (20), but presented the stimuli on a touch screen, and found that both normal rats and rats with hippocampal damage gradually acquired the task. One interpretation of these findings is that animals with hippocampal damage can partially succeed or even outperform normal animals whenever they adopt specific response to individual stimuli or stimulus compounds.…”

“…In the Dusek and Eichenbaum study (12), animals with hippocampal damage might have used other nonrelational strategies that were effective for the pairs presented in an orderly sequence (i.e., always chose the odor that was not previously rewarded, for example), but these strategies did not support performance when the order of pairs was random. In the Bussey et al study (21), the presentation of two-dimensional stimuli on a screen may have encouraged the acquisition of stimulus compounds, and that strategy may have been especially well used by animals with hippocampal damage.…”

Biphasic hemodynamic responses influence deactivation and may mask activation in block‐design fMRI paradigms

“…This problem, known as "transverse patterning," [Spence, 1952] is identical to the game "Rock Paper Scissors," in that each stimulus is ambiguous, but by attending to the relations between the stimuli, the problem can be solved. Hippocampal damage has been shown to severely disrupt performance of this task in rats [Alvarado and Rudy, 1995;Dusek and Eichenbaum, 1998; but see Bussey et al, 1998], monkeys [Alvarado et al, 2002], and humans [Reed and Squire, 1999;Rickard and Grafman, 1998], relative to a control condition in which the same stimuli are consistently designated as correct or incorrect regardless of their pairing. Hereafter, we refer to such a control condition as "elemental," while the task condition involving the transverse patterning problem is referred to as "configural" (Fig.…”