Dynamic interactions between memory systems

It has long been established that multiple memory systems, comprised of subcortical brain regions and their cortical connections, process information in unique ways, resulting in distinct strategies that can be applied to the solution of tasks. The multiple memory systems hypothesis originated from dissociations of brain area by task, and supported the idea that systems, including the hippocampus, dorsal striatum, and amygdala, operate independently. Reports of interactions between memory systems prompted organization of a symposium in 2003 and a special issue of Neurobiology of Learning and Memory in 2004, titled “Independence and interaction among memory systems.” Those reports highlighted evidence that memory systems interact with each other in cooperative and competitive manners, as well as in temporal sequence; and it heralded an important shift in research focus toward the study of interactions between memory systems. The present Special Issue of Hippocampus stems from a satellite symposium titled “Dynamic Interactions between Memory Systems,” that was held in conjunction with the 2012 Society for Neuroscience meeting in New Orleans, Louisiana. All of the papers in the current issue were authored or coauthored by investigators who participated in the symposium, and they consist of both empirical studies and theoretical reviews. In our opinion, the commentaries reflect significant advances in theoretical views of interactions among memory systems, and they provide a wealth of testable hypotheses for further advancement of the field. All the papers represent interaction of the hippocampal formation with other neural systems involved in memory, and they span a variety of approaches with human and rodent subjects across several levels of neurobiological analysis. Research reports over the past decade have shown that the memory systems approach, particularly when measured with dual solution tasks, provides an innovative perspective on learning and memory paradigms. When multiple strategies are available to individual subjects, these strategies rely on distinct brain networks. Therefore, identification of these strategies led to discoveries accounting for a significant amount of variability among research subjects. In turn, understanding these sources of variability has led to a better comprehension of underlying causal factors that explain behavior. Current findings in humans show that the hippocampus and striatal memory systems are not only involved in differential patterns of brain activity and grey matter when all individuals are tested on the same dual solution task, but also show differences in performance among patients with neurological and psychiatric disorders. The memory systems perspective is sensitive to biological factors such as genes and hormones and reveals shifts in memory systems across procedural tasks and exposure to stressors. Furthermore, this perspective shows changes across the life span that could have a significant impact on the understanding of causal factors implicated in the aging process. In the rodent, a broad array of measurements have been made from neural systems that are functionally intact, permitting investigators to examine shifts in the balance between systems during different stages of learning and memory. These measures include electrophysiological recordings, levels of energy substrates, neurotransmitters, metabolites, and the distribution and activity of signaling proteins. Among many important findings, experienceand strategy-dependent shifts in the balance of activity in neural systems that correlate with memory formation and recall have been reported. Other experiments in rodents are yielding more precise mapping of the circuitry engaged during interactions among systems that produce specific forms of learning. As is evident from the papers in this collection, a more coherent perspective of interactions among memory systems is coming into focus. With regard to the mechanics of interactions, new efforts are being made to link events at the neuronal and systems levels of analyses. The role of the prefrontal cortex in coordination of brain activity and plasticity among subcortical neural systems is being elucidated. External and internal factors that influence the relative use of one system over another are being identified and tested. Among many examples, stress is emerging as an important determinant of strategy selection, and profound implications for development and treatment of obesity, addiction, and other disorders are being articulated. The successful linkage between studies of animal models and studies using humans is evident in the number of reports in this special issue of applications of basic and mechanistic findings to mental health and other issues of social concern. *Correspondence to: Paul J. Colombo, Department of Psychology, Tulane University, New Orleans, LA 70118. E-mail: pcolomb@tulane.edu Accepted for publication 16 August 2013. DOI 10.1002/hipo.22190 Published online 22 August 2013 in Wiley Online Library (wileyonlinelibrary.com).