The well-worn route revisited: Striatal and hippocampal system contributions to route learning in human navigation

Parallel spatial memory systems theory posits that there are two types of memory system. One is a flexible, cognitive mapping system subserved by the hippocampal formation, and the other is a system centred on the striatum based on reinforcement learning principles where specific stimuli are associated with rewarded actions (O’Keefe & Nadel, 1978; White & McDonald, 2002). More recently, Khamassi & Humphries (2012) have argued that the division between model-based and model-free spatial learning is a better predictor of whether hippocampal or striatal systems will be recruited, with hippocampal systems associated with model-based responding and striatal systems with model-free responding. Model-free decision-making occurs when responding is based on average reward history associated with a particular cue-action pairing, whereas model-based decision-making allows knowledge of outcomes from previous learning history to be represented. We sought to test these theories by asking participants (N = 24) to navigate within a virtual environment through a previously learned, 9-junction route with distinctive landmarks at each junction, while undergoing functional magnetic resonance imaging. In critical conflict probe trials, a landmark was presented out of sequence such that following the usual sequence of actions would generate an opposite response to following the learned individual landmark-action association, now out of sequence. Participants that made sequence-based responses had higher parahippocampal activations relative to participants that made responses based on the individual landmark-action association, a result that would be predicted by the need to recruit model-based systems to make a sequence-based response. Parallel spatial memory systems theory would not predict hippocampal formation recruitment for either response in the conflict probe, because no cognitive mapping is required when following a prescribed route. In longer probe trials where participants were able to plan a sequence of responses, striatal systems were recruited (caudate and putamen) suggesting a role for striatum in action chunking.