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.

Keywords: dorsal striatum; habit; hippocampus; memory systems; place learning; response learning; spatial memory; stimulus-response learning.

Figure 1

Edward Chace Tolman (1886‐1959).

Figure 2

Clark Leonard Hull (1884‐1952).

Figure 3

From left to right: Kurt Lewin, Edward Tolman, and Clark Hull at the 47th Annual Meeting of the American Psychological Association in 1939. Tolman and Hull stick their tongues out at each other as a playful expression of their opposing views on learning (from the Geoffrey W. H. Leytham collection, Archives of the History of American Psychology, the Drs Nicholas and Dorothy Cummings Center for the History of Psychology, University of Akron).

Figure 4

Place and response learning in the plus-maze. (A) In the response learning plus-maze task, a rat is released from opposite start arms (e.g., N and S) throughout training, and the same body-turn response at the choice point is reinforced. For example, when the rat is released from the N arm, food is located in the W arm. When the rat is released from the S arm, food is located in the E arm. In this example, a right-body turn at the choice point is being reinforced. (B) In the place learning plus-maze task, a rat is released from opposite start arms throughout training, while the food remains in a consistently reinforced spatial location. (C) During initial training in the dual-solution plus-maze task, a rat is released from a consistent start arm (e.g., N) with food also located in a consistent spatial location (e.g., W). A rat can learn to retrieve food using a place learning strategy (i.e., go to the same place) or a response learning strategy (i.e., make the same body turn at the choice point). To determine how the rat learned to solve the task, a probe trial is conducted in which the rat is started from the opposite arm (e.g., S). If the rat continues to make the same body-turn at the choice point, the rat is labeled a response learner. If the rat makes the opposite body-turn to return to the reinforced spatial location, the rat is labeled a place learner. (D) A virtual version of the dual-solution plus-maze task may be employed to study place and response learning in human subjects (images from Astur et al., 2016). (E) Place and response learning tasks have been employed to study learning and memory across a variety of species aside from rodents and humans, including turtles, salamanders, chickens, horses, and sharks, among others (image from Salas et al., with permission from S. Karger AG, Basel).

Figure 5

Place and response learning in the eight-arm radial maze. (A) In the “win-stay” radial maze task, light cues signal whether food is available at the end of each arm. This task promotes S-R response learning to the extent that the light cues (S) become associated with approach behavior (R). (B) In the win-shift radial maze, a rat must employ extra-maze spatial cues to locate food and avoid re-entries into arms in which food was already retrieved, thus promoting the use of place learning. (C) A virtual 4/8 dual-solution version of the radial maze may be employed to examine the relative use of place and response learning in human subjects. Each trial of this task is divided into two parts (Part 1 and Part 2). During Part 1, four of the eight arms are blocked with a wall, and the participant is instructed to enter the four open arms and retrieve hidden reward objects. During Part 2, all of the arms are open, and the participant is instructed to retrieve the remaining reward objects from the arms that were previously blocked. To avoid arm re-entries, the participants may employ a place learning strategy (i.e., refer to extra-maze spatial cues to guide behavior to the correct arms) or a response learning strategy (i.e., memorizing a series of egocentric responses leading to the correct arms). During a subsequent probe trial, the extra-maze spatial cues are blocked from view, preventing the use of a place strategy. Therefore, more errors during this probe trial suggest the use of a place strategy, whereas fewer errors suggest the use of a response strategy (images from Bohbot et al., 2012). (D) A 4-year-old child searches for rewards in a place learning version of the eight-arm radial maze (image from Overman et al., 1996).

Figure 6

Place and response learning in the water maze. (A) In the cued water maze task, the platform is either visible (i.e., made of a conspicuous opaque material and/or is located above the water surface) or is cued with a proximal object (e.g., a white flag attached to the platform). Throughout training, the platform is rotated to different quadrants of the maze, and the animal must learn to associate the visible stimulus (S) with swimming approach behavior (R). (B) In the uncued spatial water maze task, the platform remains in a consistent spatial location and is visibly hidden below the water surface (the platform may consist of transparent material or the water may be infused with an opaque dye). Therefore, the rat must use extra-maze spatial cues to learn the location of the hidden platform. (C) In the dual-solution version of the water maze, a visibly cued platform remains in the same spatial location across initial training. During a later probe test, the cue is moved to a different maze quadrant. If the rat continues to swim to the same spatial location, the rat is labeled a place learner. If the rat approaches the visible cue, the rat is labeled a response learner.