Distinct error-correcting and incidental learning of location relative to landmarks and boundaries

Abstract

Associative reinforcement provides a powerful explanation of learned behavior. However, an unproven but long-held conjecture holds that spatial learning can occur incidentally rather than by reinforcement. Using a carefully controlled virtual-reality objectlocation memory task, we formally demonstrate that locations are concurrently learned relative to both local landmarks and local boundaries but that landmark-learning obeys associative reinforcement (showing ''overshadowing'' and ''blocking'' or ''learned irrelevance''), whereas boundary-learning is incidental, showing neither overshadowing nor blocking nor learned irrelevance. Crucially, both types of learning occur at similar rates and do not reflect differences in levels of performance, cue salience, or instructions. These distinct types of learning likely reflect the distinct neural systems implicated in processing of landmarks and boundaries: the striatum and hippocampus, respectively [Doeller CF, King JA, Burgess N (2008) Proc Natl Acad Sci USA 105:5915-5920]. In turn, our results suggest the use of fundamentally different learning rules by these two systems, potentially explaining their differential roles in procedural and declarative memory more generally. Our results suggest a privileged role for surface geometry in determining spatial context and support the idea of a ''geometric module,'' albeit for location rather than orientation. Finally, the demonstration that reinforcement learning applies selectively to formally equivalent aspects of task-performance supports broader consideration of two-system models in analyses of learning and decision making.associative learning ͉ blocking ͉ hippocampus ͉ overshadowing ͉ striatum

Parallel striatal and hippocampal systems for landmarks and boundaries in spatial memory

“…Our behavioral experiments (30) indicate that the striatal landmark-related learning obeys associative reinforcement with a single prediction-error signal (32,33), whereas the hippocampal boundary-related learning appears to be incidental, occurring independent of error. Thus the two systems' distinct roles may result from differences in the learning rule implemented by each and not necessarily differences in learning rate.…”

“…This finding corresponds to overshadowing of learning to the landmark by learning to the boundary in block 1: the higher the posterior hippocampal activity during block 1, the greater the influence of the boundary on responding at the start of block 2 (see ref. 30 for the corresponding behavioral experiment).…”

“…The distant orientation cues were projected at infinity so that they could be used for orientation but not location. In separate behavioral studies we formally tested the associative characteristics of learning of locations relative to the landmark or boundary within this paradigm (30).…”

Place recognition and heading retrieval are mediated by dissociable cognitive systems in mice

“…Thus, some cue competition effects may be explained by the existence of a place recognition system that is sensitive to nongeometric features. Conversely, under this interpretation, the failure of a feature to interfere with learning based on environmental geometry (49)(50)(51)(52) may indicate that the feature did not form an integral part of the representation of that place.…”

Is there a geometric module for spatial orientation? Insights from a rodent navigation model.

“…Thus, since taxon navigation in our model is based on pure S-R association learned by a reinforcement learning rule, taxon navigation should show overshadowing or blocking. Consequently, an object that was learned to be consistently located with respect to a first landmark cannot be located with respect to a second landmark that is added on, or made consistent, only later (Doeller & Burgess, 2008).…”