Nonnavigational spatial memory performance is unaffected by hippocampal damage in monkeys

Abstract

Evidence that the hippocampus is critical for spatial memory in nonnavigational tests is mixed. A recent study reported that temporary hippocampal inactivation impaired spatial memory in the nonnavigational Hamilton Search Task in monkeys. However, several studies have documented no impairment on other nonnavigational spatial memory tests following permanent hippocampal lesions. It was hypothesized that transient, but not permanent, hippocampal disruption produces deficits because monkeys undergoing transient inactivation continue to try to use a hippocampal-dependent strategy, whereas monkeys with permanent lesions use a nonhippocampal-dependent strategy. We evaluated this hypothesis by testing five rhesus monkeys with hippocampal lesions and five controls on a computerized analogue of the Hamilton Search Task. On each trial, monkeys saw an array of squares on a touchscreen, each of which "hid" one reward. Retrieving a reward depleted that location and monkeys continued selecting squares until they found all rewards. The optimal strategy is to remember chosen locations and choose each square once. Unlike the inactivation study, monkeys with hippocampal damage were as accurate as controls regardless of retention interval. Critically, we found no evidence that the groups used different strategies, as measured by learning rates, spatial search biases, perseverative win-stay errors, or inter-choice distance. This discrepancy between the effect of inactivations and lesions may result from off-target effects of inactivations or as-yet-unidentified differences between the physical and computerized tasks. Combined with previous evidence that hippocampal damage impairs navigational memory in monkeys, this evidence constrains the role of the hippocampus in spatial memory as being critical for navigational tests that likely involve allocentric spatial memory but not nonnavigational tests that likely involve egocentric spatial memory.