Neurobehavioral evidence supports the existence of at least two anatomically distinct "memory systems" in the mammalian brain that mediate dissociable types of learning and memory; a "cognitive" memory system dependent upon the hippocampus and a "stimulus-response/habit" memory system dependent upon the dorsolateral striatum. Several findings indicate that despite their anatomical and functional distinctiveness, hippocampal-and dorsolateral striataldependent memory systems may potentially interact and that, depending on the learning situation, this interaction may be cooperative or competitive. One approach to examining the neural mechanisms underlying these interactions is to consider how various factors influence the relative use of multiple memory systems. The present review examines several such factors, including information compatibility, temporal sequence of training, the visual sensory environment, reinforcement parameters, emotional arousal, and memory modulatory systems. Altering these parameters can lead to selective enhancements of either hippocampal-dependent or dorsolateral striatal-dependent memory, and bias animals toward the use of either cognitive or habit memory in dual-solution tasks that may be solved adequately with either memory system. In many learning situations, the influence of such experimental factors on the relative use of memory systems likely reflects a competitive interaction between the systems. Research examining how various factors influence the relative use of multiple memory systems may be a useful method for investigating how these systems interact with one another. V C 2013 Wiley Periodicals, Inc.

The view that anatomically distinct memory systems differentially contribute to the development of drug addiction and relapse has received extensive support. The present brief review revisits this hypothesis as it was originally proposed 20 years ago (1) and highlights several recent developments. Extensive research employing a variety of animal learning paradigms indicates that dissociable neural systems mediate distinct types of learning and memory. Each memory system potentially contributes unique components to the learned behavior supporting drug addiction and relapse. In particular, the shift from recreational drug use to compulsive drug abuse may reflect a neuroanatomical shift from cognitive control of behavior mediated by the hippocampus/dorsomedial striatum toward habitual control of behavior mediated by the dorsolateral striatum (DLS). In addition, stress/anxiety may constitute a cofactor that facilitates DLS-dependent memory, and this may serve as a neurobehavioral mechanism underlying the increased drug use and relapse in humans following stressful life events. Evidence supporting the multiple systems view of drug addiction comes predominantly from studies of learning and memory that have employed as reinforcers addictive substances often considered within the context of drug addiction research, including cocaine, alcohol, and amphetamines. In addition, recent evidence suggests that the memory systems approach may also be helpful for understanding topical sources of addiction that reflect emerging health concerns, including marijuana use, high-fat diet, and video game playing.

Extensive evidence indicates that mammalian memory is organized into multiple brains systems, including a “cognitive” memory system that depends upon the hippocampus and a stimulus-response “habit” memory system that depends upon the dorsolateral striatum. Dorsal striatal-dependent habit memory may in part influence the development and expression of some human psychopathologies, particularly those characterized by strong habit-like behavioral features. The present review considers this hypothesis as it pertains to psychopathologies that typically emerge during childhood and adolescence. These disorders include Tourette syndrome, attention-deficit/hyperactivity disorder, obsessive-compulsive disorder, eating disorders, and autism spectrum disorders. Human and nonhuman animal research shows that the typical development of memory systems comprises the early maturation of striatal-dependent habit memory and the relatively late maturation of hippocampal-dependent cognitive memory. We speculate that the differing rates of development of these memory systems may in part contribute to the early emergence of habit-like symptoms in childhood and adolescence. In addition, abnormalities in hippocampal and striatal brain regions have been observed consistently in youth with these disorders, suggesting that the aberrant development of memory systems may also contribute to the emergence of habit-like symptoms as core pathological features of these illnesses. Considering these disorders within the context of multiple memory systems may help elucidate the pathogenesis of habit-like symptoms in childhood and adolescence, and lead to novel treatments that lessen the habit-like behavioral features of these disorders.

Emotional arousal induced by stress and/or anxiety can exert complex effects on learning and memory processes in mammals. Recent studies have begun to link study of the influence of emotional arousal on memory with earlier research indicating that memory is organized in multiple systems in the brain that differ in terms of the “type” of memory they mediate. Specifically, these studies have examined whether emotional arousal may have a differential effect on the “cognitive” and stimulus-response “habit” memory processes sub-served by the hippocampus and dorsal striatum, respectively. Evidence indicates that stress or the peripheral injection of anxiogenic drugs can bias animals and humans toward the use of striatal-dependent habit memory in dual-solution tasks in which both hippocampal and striatal-based strategies can provide an adequate solution. A bias toward the use of habit memory can also be produced by intra-basolateral amygdala (BLA) administration of anxiogenic drugs, consistent with the well documented role of efferent projections of this brain region in mediating the modulatory influence of emotional arousal on memory. In some learning situations, the bias toward the use of habit memory produced by emotional arousal appears to result from an impairing effect on hippocampus-dependent cognitive memory. Further research examining the neural mechanisms linking emotion and the relative use of multiple memory systems should prove useful in view of the potential role for maladaptive habitual behaviors in various human psychopathologies.

In lower animals and humans, stress/anxiety can enhance dorsal striatal-dependent habit memory,at the expense of hippocampal-dependent cognitive memory. The present review considers the potential for this 'stress/anxiety-induced habit bias' to explain some aspects of post-traumatic stress disorder (PTSD). In rats,anxiety induced by peripheral or intra-amygdala infusions of anxiogenic drugs can enhance habit memory and impair cognitive memory. In tasks in which both habit and cognitive memory processes may provide a learned solution, stress and drug-induced anxiety favors the use of habit memory. The effect of stress and anxiety on the use of multiple memory systems in rats depends on the functional integrity of the basolateral amygdala. Thus,under robust emotional arousal, amygdala activation can modulate the relative use of memory systems in a manner that favors habit memory. We propose a similar mechanism may underlie the development and persistence of some PTSD symptoms. The traumatic memories of PTSD patients can be deficient in hippocampus-dependent contextual or autobiographical aspects, and enhanced in responding to trauma-related cues, which we suggest may reflect increased involvement of the dorsal striatum.We briefly consider the potential role of a stress/anxiety induced habit bias with regard to other psychopathologies,including obsessive-compulsive disorder and drug addiction.

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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.

The view that different kinds of memory are mediated by dissociable neural systems has received extensive experimental support. Dissociations between memory systems are usually observed during initial acquisition, consolidation, and retrieval of memory, however increasing evidence also indicates a role for multiple memory systems in extinction behavior. The present article reviews a recent series of maze learning experiments that provide evidence for a multiple memory systems approach to extinction learning and memory. Evidence is described indicating that: (1) the hippocampus and dorsolateral striatum (DLS) mediate different kinds of extinction learning; (2) the effectiveness of different extinction protocols depends on the kind of memory being extinguished; and (3) whether a neural system is involved in extinction is also determined by the extinction protocol and kind of memory undergoing extinction. Based on these findings, a novel hypothetical model regarding the role of multiple memory systems in extinction is presented. In addition, the relevance of this multiple memory systems approach to other learning paradigms involving extinction (i.e., extinction of conditioned fear) and for treating human psychopathologies characterized by maladaptive memories (e.g., drug addiction and relapse) is briefly considered.