A secondary working memory challenge preserves primary place strategies despite overtraining

Abstract

Learning by repetition engages distinct cognitive strategies whose contributions are adjusted with experience. Early in learning, performance relies upon flexible, attentive strategies. With extended practice, inflexible, automatic strategies emerge. This transition is thought fundamental to habit formation and applies to human and animal cognition. In the context of spatial navigation, place strategies are flexible, typically employed early in training, and rely on the spatial arrangement of landmarks to locate a goal. Response strategies are inflexible, become dominant after overtraining, and utilize fixed motor sequences. Although these strategies can operate independently, they have also been shown to interact. However, since previous work has focused on single-choice learning, if and how these strategies interact across sequential choices remains unclear. To test strategy interactions across sequential choices, we utilized various two-choice spatial navigation tasks administered on the Opposing Ts maze, an apparatus for rodents that permits experimental control over strategy recruitment. We found that when a second choice required spatial working memory, the transition to response navigation on the first choice was blocked. Control experiments specified this effect to the cognitive aspects of the secondary task. In addition, response navigation, once established on a single choice, was not reversed by subsequent introduction of a secondary choice reliant on spatial working memory. These results demonstrate that performance strategies interact across choices, highlighting the sensitivity of strategy use to the cognitive demands of subsequent actions, an influence from which overtrained rigid actions may be protected.[Supplemental material is available for this article.]Whenever a subject engages in a repetitive task or behavior, with practice several aspects of performance undergo modification. Not only does overall performance tend to improve or become more effective, but the underlying cognitive strategies change. Specifically, the formation of habits is thought to result from an incremental progression away from the use of flexible, attentive performance strategies to the engagement of inflexible, automatic strategies. This strategy transition is observed in various cognitive domains, e. . Although the transition is robust, several factors internal and external to the subject alter the onset of automatic behaviors (Restle 1957;McDonald et al. 2004;Packard 2009). These factors seem to exert their effects by differentially engaging dissociable learning and memory systems which interact to recruit a distinct performance strategy at select time points during learning. Thus, an understanding of these interactions has important implications for decision-making at large.Much of the current evidence for the nature of these interactions stems from studies of spatial navigation. In these studies, flexible/attentive strategies, termed place (locale) strategies, rely on calibrated spatial information associated with ...

Hippocampus and subregions of the dorsal striatum respond differently to a behavioral strategy change on a spatial navigation task

“…This behavioral phenomenon is termed vicarious trial-and-error (VTE) behavior and has been hypothesized to reflect an underlying search process Muenzinger 1938;Tolman 1938). VTE primarily occurs during goal-directed behaviors (Gardner et al 2013;Papale et al 2012;Schmidt et al 2013;Tolman 1938).…”

Differential Arc expression in the hippocampus and striatum during the transition from attentive to automatic navigation on a plus maze

“…1). We used a previously described multi-choice maze (the Opposing T’s: OpT maze) set in a plus maze configuration (see Gardner et al, 2013; minor modifications are detailed). Briefly, four arm segments (north, east, south, and west) built off a central square (choice/decision point) were utilized.…”

“…Food restriction and habituation were largely implemented as previously described (Gardner et al, 2013). Rats were individually-housed and maintained at 85% of their free-feeding weight throughout the experiment.…”

“…All training and probe trials were videotaped for analysis. Vicarious trial and error (VTE) was quantified on each probe run by summing the number of times a rat paused at the decision point of the maze and the number of times it partially entered the east and west arms prior to making a full entry (e.g., see Gardner et al, 2013). …”

“…VTE refers to the tendency for rats to pause at a choice point and look back and forth toward potential destinations (Muenzinger, 1938; Muenzinger & Gentry, 1931; Tolman, 1948). As VTE is associated with deliberation (Papale, Stott, Powell, Regier, & Redish, 2012; van der Meer, Kurth-Nelson, & Redish, 2012) and place navigation (Gardner et al, 2013; Schmidt, Papale, Redish, & Markus, 2013), and correlated with hippocampal metabolism (Hu, Xu, & Gonzalez-Lima, 2006), this behavioral measure may further clarify the degree to which attentive systems are recruited during task repetition.…”