PLACE VERSUS RESPONSE LEARNING REVISITED IN THE BRAIN

A chief concern of learning and memory researchers involves determining what is learned in a given situation. Edward L. Thorndike (1933) was an early proponent of the view that animals learn associations between stimuli and responses (i.e., S-R learning), and in his influential law of effect, Thorndike essentially proposed that S-R associations were strengthened by reinforcement (a satisfying event) and weakened by nonreinforcement (an annoying event). In Thorndike's laboratory investigation of the learning abilities of several animal species, the learning curves that he observed were gradual; he therefore argued that learning was not akin to intuition or the sudden illumination of a light bulb. Rather, learning appeared to be an incremental process of trial-and-error, resulting in the eventual acquisition of S-R associations. Thorndike's early S-R learning theory and the rise of James B. Watson's psychological behaviorism influenced the subsequent work of the psychologist Clark L. Hull, who introduced fairly elaborate mathemati cal formulas in his description of a S-R habit learning theory (Hull, 1943).

Edward C. Tolman was an early proponent of a different theoretical approach to understanding learned behavior. Tolman (1932) argued that S-R theory did not adequately explain all learning phenomena; he suggested instead that animals acquire expectations about how various behaviors would lead to a desired goal. Tolman used terms such as inference, intention, and purpose to explain learned behavior. His views on animal learning were perhaps most clearly defined in his hypothesis that animals form a cognitive map of the environment in which spatial relationships among multiple stimuli are represented in memory and could be used to guide goal-directed behavior.

The Plus-Maze Task and the Behaviorist versus Cognitivist Debate

A significant empirical battle flared between S-R behaviorist and cognitive-learning theorists, and involved the investigation of behavior in several learning tasks. One task that employed a plus-maze apparatus can illustrate these two approaches to understanding what animals learn (Tolman, Ritchie, and Kalish, 1946). The plus-maze is essentially two T-mazes arranged so that a goal box (e.g., east or west), can be approached from one of two start boxes (e.g., north or south). In one version of the task, rats are trained over trials to obtain food from a consistently baited goal box (e.g., west), from the same start box (e.g., south). According to S-R learning theory, rats can learn to approach the baited goal box by acquiring a response tendency (i.e., a specific body turn at the choice point). In contrast, according to cognitive learning theory, rats trained in this task learn the place or spatial location of the reinforcer, and this expectation can guide an approach response to the baited goal box.

Both behaviorist and cognitive learning theories can adequately explain the acquisition of this version of the plus-maze task. However, a probe trial in which trained rats are given a trial starting from the opposite start box (e.g., north) can assess the type of information acquired. Rats with knowledge of the spatial location of the reinforcer should continue to approach the baited goal box on the probe trial (i.e., place learning), whereas rats that have learned a specific body turn should choose the opposite goal box on the probe trial (i.e., response learning). In their early research, Tolman and colleagues demonstrated that rats trained in a plus-maze to approach a goal box from the same start point on each trial could indeed display place learning when probe trial behavior was later assessed. In addition, rats can acquire place learning in a version of the plus-maze task in which they are trained to approach the same goal arm (e.g., west) from two different starting points (e.g., north and south). In this version of the task, rats are required to make a different body turn at the maze choice point (i.e., left or right), depending on the start position; therefore response learning would be ineffective for acquiring the task.

Taken together, these demonstrations of place learning in the plus-maze suggest that S-R theories may not adequately explain all types of learning. However, subsequent research revealed that in addition to place learning, rats could also use response learning in acquiring plus-maze behavior. For example, under some experimental conditions, rats trained to approach the same goal arm (e.g., west) from a consistent starting point (e.g., south), tended to display response learning on a subsequent probe trial. Moreover, rats can acquire response learning in a version of the plus-maze task in which they are trained from two different starting points (e.g., north and south) and are required to make a consistent body turn response (e.g., turn left) at the maze choice point. In an influential review of the plus-maze literature, Restle suggested that the relative use of place and response learning depends on various experimental factors, most critically the availability of intraand extra-maze cues (Restle, 1957). For example, environments in which various distal extra-maze cues are present favor place learning, whereas the use of sparsely cued extra-maze environments favor response learning.

Neurobiology of Memory Organization and the Behaviorist versus Cognitivist Debate

Although the plus-maze task appeared to hold early promise for resolving the dispute between behaviorists and cognitive theorists in favor of one theoretical viewpoint, the findings of various plus-maze studies clearly indicated that brain-intact rats are capable of both place and response learning. However, contemporary behavioral neuroscience research suggests a possible resolution of this debate. Research has revealed that mammalian memory is organized in relatively independent brain systems that differ in the types of memory they mediate (Hirsh, 1974; O'Keefe and Nadel, 1978; Cohen and Squire, 1980; Mishkin and Petri, 1984; Eichenbaum and Cohen, 2001). There is evidence that the hippocampus is part of a memory system that mediates cognitive memory, whereas the caudate-putamen is part of a memory system that mediates stimulus-response or habit memory (e.g., Packard, Hirsh, and White, 1989; Fernandez-Ruiz et al., 2001). The multiple-memory-systems hypothesis raises the interesting possibility that place and response learning may in fact have distinct neural substrates, suggesting that a neurobiologically based approach may help to address the differing viewpoints of S-R and cognitive-learning theorists (Mishkin and Petri, 1984).

Multiple Memory Systems and the Place versus Response Learning Debate

A plus-maze study was designed to differentiate the mnemonic roles of the hippocampus and caudateputamen (Packard and McGaugh, 1996). In this study rats were trained in a daily session to obtain food from a consistently baited goal box and were allowed to approach this maze arm from the same starting box on each trial. Following seven days of training, rats were given a probe trial to determine whether they had acquired the task using place information or had learned a specific body-turn response. Prior to the probe trial, rats received intrahippocampal or intracaudate infusions of a vehicle solution or lidocaine, an anesthetic that produces a temporary inactivation of neural function in the affected brain region. On the probe trial, rats receiving vehicle infusions into the hippocampus or caudate-putamen were predominantly place learners. Lidocaine infused into the hippocampus blocked expression of place learning, whereas similar infusions into the caudate-putamen did not. Therefore, the functional integrity of the hippocampus but not caudate-putamen is necessary for the expression of place learning. Following extended training in the plus-maze, rats given a second probe trial switch from place learning to response learning (Ritchie, Aeschliman, and Pierce, 1950; Hicks, 1964). Therefore, in the study by Packard and McGaugh (1996), the rats were trained for an additional seven days, given a second probe trial on the sixteenth day, and again received intracerebral infusions of lidocaine prior to the probe trial. On this second probe trial rats receiving vehicle infusions into either the hippocampus or caudate-putamen were predominantly response learners, providing evidence of a switch from place to response learning tendencies with extended training.

On the second probe trial, intrahippocampal infusions of lidocaine did not block the expression of response learning. However, rats receiving intracaudate infusions of lidocaine prior to the second probe trial exhibited place learning, demonstrating a blockade of the expression of response learning. Taken together, these findings demonstrate a double dissociation between the roles of the hippocampus and caudate-putamen in place and response learning, respectively. Moreover, when the shift from the use of place to response learning occurs, the hippocampus-dependent place representation is not extinguished or forgotten. Rather, at a time in training in which animals predominantly use response learning, the place representation can be brought back into use or "un-masked" by a blockade of the caudate-putamen response learning system.

The shift in the use of a hippocampus-dependent place strategy to a caudate-dependent response strategy suggests that in a learning task in which both memory systems can provide an adequate solution, the hippocampal system mediates a rapid cognitive form of learning that initially guides behavior, whereas the caudate-putamen mediates a more slowly developing S-R or habit form of learning that eventually guides learned behavior. This raises the intriguing possibility that infusions of memory-enhancing drugs into these two brain structures during early training might influence the time-course of this shift. In an experiment designed to address this possibility, rats received posttraining intrahippocampal or intracau-date infusions of the amino acid neurotransmitter glutamate during early time points in cross-maze training (Packard, 1999). As observed previously, rats receiving saline control injections predominantly displayed place learning on an early (day eight) probe trial, and response learning on a later (day sixteen) probe trial. However, rats receiving posttraining intrahippocampal infusions of glutamate predominantly displayed place learning on both the early and late probe trials, suggesting that infusion of glutamate into the hippocampus strengthened a place learning representation and prevented the shift to response learning that occurs with extended training. In contrast, rats given posttraining glutamate infusions into the caudate-putamen predominantly displayed response learning on both the early and late probe trials, suggesting that infusion of glutamate into the caudate-putamen accelerated the shift to response learning that is normally observed with extended behavioral training.

The findings from behavioral neuroscience research employing brain lesion and intracerebral drug infusion techniques provide a partial neurobiological resolution of the place versus response learning debate. Whereas previous research clearly demonstrates that brain-intact animals are capable of both place and response learning (Restle, 1957), such behaviors do not reflect a single learning and memory system. Rather, distinct neuroanatomical substrates that include the hippocampus and caudate-putamen mediate the acquisition of place and response learning, respectively. Thus, four decades after the introduction of the plus-maze task as a means of addressing the fundamental question of what animals learn in a given situation, the mammalian brain appears to have spoken in favor of the viewpoint that the historic debate between S-R and cognitive learning theorists may in part have been misguided in to impose a single theoretical viewpoint on all types of learning.

See also:GUIDE TO THE ANATOMY OF THE BRAIN: HIPPOCAMPUS AND PARAHIPPOCAMPAL REGION

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Mark G.Packard