Conflict between place and response navigation strategies: Effects on vicarious trial and error (VTE) behaviors

Schmidt, Brandy; Papale, Andrew E.; Redish, A. David; Markus, Etan J.

doi:10.1101/lm.028753.112

Cited by 67 publications

(104 citation statements)

References 28 publications

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“…Similar to the alternation of navigational strategies strategies observed in rodents 5 , the levels of IdPhi scoring in our experiment were significantly higher for the high-frequency condition when compared to the low-frequency condition. Therefore, it not only suggests that participants adapt their strategies to the experimental contingency but also rejects the hypothesis that participants relied on a memory of action sequences in the low-frequency condition.…”

Section: Discussionsupporting

confidence: 70%

“…We hypothesized that humans benefit from behavioral correlates of spatial decision-making, specifically from VTE behaviors, as has been previously shown in rodents 1, 2,5,16 In order to measure whether humans do benefit from these back and forth head-scanning behaviors, we quantified navigational variables in both high and low-frequency conditions. Because highfrequency conditions have, by definition, a greater probability of occurring, we expected that trajectory length and duration of trials with high-frequency start-target combinations would be shorter when compared with low-frequency conditions.…”

Section: Vtementioning

confidence: 99%

“…The IdPhi measure has been used in the rodent literature to quantify VTE behaviors at decision-points of navigational tasks 5 . We adapted IdPhi to our dataset in order to quantify changes in angular orientation at decision-points during navigation.…”

Section: Idphi: Vte Behaviormentioning

confidence: 99%

“…Specifically, lidocaine inactivation of hippocampal neural populations impaired "place" strategies and striatal caudate nucleus inactivation disrupted "response" navigational strategies 7 . The distinct recruitment of these brain regions during spatial navigation suggests that with increased familiarity, initial learning stages, when tasks still require the association of spatial and sensorial information for the understanding of the experimental contingency, progressively transition into a cue-action coding scheme 5 .…”

Section: Introductionmentioning

confidence: 99%

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Human vicarious trial and error is predictive of spatial navigation performance

Santos-Pata

Verschure

2018

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When learning new environments, rats often pause at decision points and look back and forth over their possible trajectories as if they were imagining the future outcome of their actions, a behavior termed "Vicarious trial and error" (VTE). As the animal learns the environmental configuration, rats change from deliberative to habitual behavior, and VTE tends to disappear, suggesting a functional relevance in the early stages of learning. Despite the extensive research on spatial navigation, learning and VTE in the rat model, fewer studies have focused on humans. Here, we tested whether head-scanning behaviors that humans typically exhibit during spatial navigation are as predictive of spatial learning as in the rat. Subjects performed a goal-oriented virtual navigation task in a symmetric environment. Spatial learning was assessed through the analysis of trajectories, timings, and head orientations, under habitual and deliberative spatial navigation conditions. As expected, we found that trajectory length and duration decreased with the trial number, implying that subjects learned the spatial configuration of the environment over trials. Interestingly, IdPhi (a standard metric of VTE) also decreased with the trial number, suggesting that humans benefit from the same head-orientation scanning behavior as rats at spatial decision-points. Moreover, IdPhi captured exclusively at the first decision-point of each trial, was correlated with trial trajectory duration and length. Our findings demonstrate that in VTE is a signature of the stage of spatial learning in humans, and can be used to predict performance in navigation tasks with high accuracy.

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Section: Discussionsupporting

confidence: 70%

Section: Vtementioning

confidence: 99%

Section: Idphi: Vte Behaviormentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Human vicarious trial and error is predictive of spatial navigation performance

Santos-Pata

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2018

Preprint

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“…This has been interpreted as a signature of cognitive search and deliberation between the two choices (i.e., going right or left). In keeping with a role of VTE behavior for deliberation, it occurs early in learning and decreases or disappears after significant experience (Tolman 1939;van der Meer and Redish 2010;van der Meer et al 2012) but it can increase again when task contingencies change (Blumenthal et al 2011;Schmidt et al 2013;Regier et al 2015). VTE behavior has been consistently linked to hippocampal function (Hu and Amsel 1995;Voss et al 2011;Regier et al 2015).…”

mentioning

confidence: 99%

Active Inference, epistemic value, and vicarious trial and error

et al. 2016

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Balancing habitual and deliberate forms of choice entails a comparison of their respective merits-the former being faster but inflexible, and the latter slower but more versatile. Here, we show that arbitration between these two forms of control can be derived from first principles within an Active Inference scheme. We illustrate our arguments with simulations that reproduce rodent spatial decisions in T-mazes. In this context, deliberation has been associated with vicarious trial and error (VTE) behavior (i.e., the fact that rodents sometimes stop at decision points as if deliberating between choice alternatives), whose neurophysiological correlates are "forward sweeps" of hippocampal place cells in the arms of the maze under consideration. Crucially, forward sweeps arise early in learning and disappear shortly after, marking a transition from deliberative to habitual choice. Our simulations show that this transition emerges as the optimal solution to the trade-off between policies that maximize reward or extrinsic value (habitual policies) and those that also consider the epistemic value of exploratory behavior (deliberative or epistemic policies)-the latter requiring VTE and the retrieval of episodic information via forward sweeps. We thus offer a novel perspective on the optimality principles that engender forward sweeps and VTE, and on their role on deliberate choice.Substantial evidence indicates that animal behavior is determined both by deliberative processes (i.e., based on predictions of future outcomes and rewards) and by habitual reflexes (i.e., based on stimulus-response associations; Balleine and Dickinson 1998). The former are more resource intensive and sensitive to changes in task contingencies, while the latter are cheaper but inflexible; hence whether it is optimal to call on deliberative or habitual choice depends on the trade-off between the advantage of flexibility and computational costs (Balleine and Dickinson 1998;Dolan and Dayan 2013;Lee et al. 2014). In this paper, we try to understand the contextualization of behavior and the trade-off between deliberative and habitual choice from first principles, using Active Inference and Markov decision process models of exploitation and exploration (Friston et al. 2013(Friston et al. , 2014Pezzulo et al. 2015).We focus specifically on vicarious trial and error (VTE) behavior, which is considered a hallmark of deliberation (Muenzinger 1938;Tolman 1938Tolman , 1939. This is based on the observation that, when rodents have to remember or search the correct route to a reward in a maze (e.g., a T-maze), they sometimes stop at choice points, to look left and right before choosing which direction to go. This has been interpreted as a signature of cognitive search and deliberation between the two choices (i.e., going right or left). In keeping with a role of VTE behavior for deliberation, it occurs early in learning and decreases or disappears after significant experience (Tolman 1939;van der Meer and Redish 2010;van der Meer et al. 2012) but it can incr...

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Interindividual differences in memory system local field potential activity predict behavioral strategy on a dual‐solution T‐maze

et al. 2020

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Individuals can use diverse behavioral strategies to navigate their environment including hippocampal-dependent place strategies reliant upon cognitive maps and striatal-dependent response strategies reliant upon egocentric body turns. The existence of multiple memory systems appears to facilitate successful navigation across a wide range of environmental and physiological conditions. The mechanisms by which these systems interact to ultimately generate a unitary behavioral response, however, remain unclear. We trained 20 male, Sprague-Dawley rats on a dual-solution T-maze while simultaneously recording local field potentials that were targeted to the dorsolateral striatum and dorsal hippocampus. Eight rats spontaneously exhibited a place strategy while the remaining 12 rats exhibited a response strategy. Interindividual differences in behavioral strategy were associated with distinct patterns of LFP activity between the dorsolateral striatum and dorsal hippocampus. Specifically, striatalhippocampal theta activity was in-phase in response rats and out-of-phase in place rats and response rats exhibited elevated striatal-hippocampal coherence across a wide range of frequency bands. These contrasting striatal-hippocampal activity regimes were (a) present during both maze-learning and a 30 min premaze habituation period and (b) could be used to train support vector machines to reliably predict behavioral strategy. Distinct patterns of neuronal activity across multiple memory systems, therefore, appear to bias behavioral strategy selection and thereby contribute to interindividual differences in behavior.

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Conflict between place and response navigation strategies: Effects on vicarious trial and error (VTE) behaviors

Cited by 67 publications

References 28 publications

Human vicarious trial and error is predictive of spatial navigation performance

Human vicarious trial and error is predictive of spatial navigation performance

Active Inference, epistemic value, and vicarious trial and error

Interindividual differences in memory system local field potential activity predict behavioral strategy on a dual‐solution T‐maze

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