Place vs. Response Learning: History, Controversy, and Neurobiology

Abstract

The present article provides a historical review of the place and response learning plus-maze tasks with a focus on the behavioral and neurobiological findings. The article begins by reviewing the conflict between Edward C. Tolman’s cognitive view and Clark L. Hull’s stimulus-response (S-R) view of learning and how the place and response learning plus-maze tasks were designed to resolve this debate. Cognitive learning theorists predicted that place learning would be acquired faster than response learning, indicating the dominance of cognitive learning, whereas S-R learning theorists predicted that response learning would be acquired faster, indicating the dominance of S-R learning. Here, the evidence is reviewed demonstrating that either place or response learning may be dominant in a given learning situation and that the relative dominance of place and response learning depends on various parametric factors (i.e., amount of training, visual aspects of the learning environment, emotional arousal, et cetera). Next, the neurobiology underlying place and response learning is reviewed, providing strong evidence for the existence of multiple memory systems in the mammalian brain. Research has indicated that place learning is principally mediated by the hippocampus, whereas response learning is mediated by the dorsolateral striatum. Other brain regions implicated in place and response learning are also discussed in this section, including the dorsomedial striatum, amygdala, and medial prefrontal cortex. An exhaustive review of the neurotransmitter systems underlying place and response learning is subsequently provided, indicating important roles for glutamate, dopamine, acetylcholine, cannabinoids, and estrogen. Closing remarks are made emphasizing the historical importance of the place and response learning tasks in resolving problems in learning theory, as well as for examining the behavioral and neurobiological mechanisms of multiple memory systems. How the place and response learning tasks may be employed in the future for examining extinction, neural circuits of memory, and human psychopathology is also briefly considered.

Apparatus design and behavioural testing protocol for the evaluation of spatial working memory in mice through the spontaneous alternation T-maze

“…By rotating the maze 180°, the T-maze can indeed be used as a cross (or plus maze). The place/response cross maze task, originally conceived by Tolman in the 1940s 44 , 45 and resumed by Mark Packard and James McGaugh in the mid 1990s 46 , 47 , is one of the most efficient tools to evaluate place versus response learning 48 . In this procedure the experimenter releases the animals in the inferior arm of a cross maze surrounded by specific environmental visual cues and trains them to find a food reward which is constantly placed in one defined lateral arm (for example the right one), while keeping closed the two remaining arms (left and superior).…”

“…For instance, a T-maze with open arms or enclosed arms with transparent walls allows allocentric orientation, while in a maze with high obscured walls impeding the vision of distal cues and where no intra-maze cues are present the egocentric strategy will be promoted. Indeed, it has been shown that in environments with abundant extra-maze stimuli, the allocentric place strategy is preferred over the egocentric response strategy, while the opposite is true in environments with few or no extra-maze cues 48 .…”

Enhanced Hippocampus-Nidopallium Caudolaterale Connectivity during Route Formation in Goal-Directed Spatial Learning of Pigeons

“…Secondly, this study did not examine and explain the relationship of the two different potential mechanisms for the spatial learning of the pigeons. There are two broadly opposing views regarding the mechanisms of animal spatial learning, namely response learning using a stimulus-response strategy and place learning using a cognitive strategy [45]. Current studies have suggested that spatial information is slowly incorporated into the optimal behavioral response in spatial learning [10], and response-and place-based frames may cooperate during route formation [46].…”

A Quantitative Framework for Identifying Patterns of Route-Use in Animal Movement Data

“…Unfortunately, this conceptualization does not explain the differences between patterns generated by oriented mechanisms and memory mechanisms, or the variation in patterns generated by different memory systems such as response learning and place learning. In response learning (see Glossary; reviewed in Goodman, 2021), behavioral responses to specific cues (landmarks) are reinforced if they lead to rewards such as food. Under this mechanism, animals may develop habitual sequences of spatial behavior, such as traplines, without needing to model or "map" their environment.…”

“…Under this mechanism, animals may develop habitual sequences of spatial behavior, such as traplines, without needing to model or "map" their environment. Alternatively, with place learning (see Glossary; reviewed in Goodman, 2021), animals may learn the distances and directions between important locations and plan routes between them. Often referred to as a "cognitive map, " consistent decision-making with the use of place learning may lead to routeformation, but the use of the memory mechanism by animals remains debated.…”