The Speed of Associative Learning and Retrieval in Humans and Non-Human Primates

Abstract

The conversion of a memory from an initially fragile state to an enduring representation requires cellular, molecular, and systems-level brain network changes. This reorganization is hypothesized to involve time-dependent neuroanatomical changes that may differentially support some types of remote versus recent memory, and may also influence the latency to decide and complete responses during retrieval. To quantify the timecourse of learning and retrieval after different retention durations, a paradigm is developed to measure in humans and monkeys the retrieval speed of visuomotor associations, which require an intact hippocampus for initial acquisition but not for retrieval after days or weeks. Two components of retrieval speed, a decision time to initiate movement and a velocity-dependent movement completion time to complete a motor response, are shown to change differently relative to a pre-retention baseline. Movement completion times decrease across repetitions within single learning session, and continue to decrease from the level reached at the end of learning following retention. Decision times also decrease within the learning session, but increase on the first post-retention retrieval attempt as a function of retention interval duration. Extensive practice is required for decision times to reach a level below that obtained at the end of learning, and the transition from a long- to short-latency decision depends on the number and spacing of practice trials. The findings are discussed in a framework in which post-retention processing time is influenced by the speed of visual identification, the time to retrieve the associative relationship from long-term memory, and the time to plan and execute a motor response. The creation of sparser, long-lasting visual form representations and strengthened cortico-striatal connections predict behavioral efficiency gains in visual identification and motor responses after learning. Decision times could be fast and automatic following extensive practice when the neural representation may become stored permanently in cortico-cortical and cortico-striatal linkages, or could increase after retention because of several cognitive and neural factors, including interference and frontal inhibition of the hippocampal system to prevent new learning before choice feedback. The experimental results are discussed in the context of the existing literature on memory consolidation.