Review
The role of the basal ganglia in learning and memory: Insight from Parkinson’s disease

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Abstract

It has long been known that memory is not a single process. Rather, there are different kinds of memory that are supported by distinct neural systems. This idea stemmed from early findings of dissociable patterns of memory impairments in patients with selective damage to different brain regions. These studies highlighted the role of the basal ganglia in non-declarative memory, such as procedural or habit learning, contrasting it with the known role of the medial temporal lobes in declarative memory. In recent years, major advances across multiple areas of neuroscience have revealed an important role for the basal ganglia in motivation and decision making. These findings have led to new discoveries about the role of the basal ganglia in learning and highlighted the essential role of dopamine in specific forms of learning. Here we review these recent advances with an emphasis on novel discoveries from studies of learning in patients with Parkinson’s disease. We discuss how these findings promote the development of current theories away from accounts that emphasize the verbalizability of the contents of memory and towards a focus on the specific computations carried out by distinct brain regions. Finally, we discuss new challenges that arise in the face of accumulating evidence for dynamic and interconnected memory systems that jointly contribute to learning.

Highlights

► The basal ganglia contribute to specific kinds of learning and memory. ► Parkinson’s disease is a useful model of the basal ganglia’s role in human learning. ► Findings across species lead to novel insights into basal ganglia learning mechanisms. ► Basal ganglia and medial temporal lobe system functions are often contrasted. ► Current theories emphasize computations, rather than verbalizability, of each system.

Introduction

Research on the neurobiology of learning and memory has lead to the proposal that different forms of memory are supported by different brain structures. A focus of research within this framework is to determine which structures contribute to which mnemonic processes; for example, double dissociation studies aim to tease apart unique patterns of brain activity in response to different tasks. The division of long-term memory into declarative and non-declarative processes has been one such fruitful dissociation (Cohen and Eichenbaum, 1993, Gabrieli, 1998, Knowlton et al., 1996, Squire and Zola, 1996).

This basic division of mnemonic function has provided a powerful framework for understanding the organization of memory in the brain. It has led to major advances in understanding the role of the medial temporal lobes in declarative memory and has indicated a separate role for the basal ganglia in habit learning, a form of non-declarative memory. However, by defining the role of the basal ganglia in contrast to that of the medial temporal lobe, the framework has left many important questions unanswered: What are the mechanisms by which learning takes place in the basal ganglia and in its subregions? What are the factors that modulate such learning? Do the basal ganglia and medial temporal lobes operate as independent systems, or do they interact?

Researchers have just begun to address these questions, stimulated by a convergence of evidence from systems and computational neuroscience regarding the role of the basal ganglia (primarily the dorsal and ventral striatum) and their dopaminergic inputs in learning to predict rewards and acting to obtain them. Here, we review these recent advances with an eye towards providing an integrated account of the role of the basal ganglia in learning, a role where the basal ganglia not only acts independently from other brain regions, but also in interaction with them.

Section snippets

Multiple memory systems: understanding the role of the basal ganglia

Extensive converging evidence indicates that long-term memory is not unitary, but instead consists of multiple cognitive processes that rely on discrete neural systems and are governed by distinct learning rules and forms of plasticity (Gabrieli, 1998, Squire and Zola, 1996, White and McDonald, 2002). This concept, often referred to as the multiple memory systems framework, originated from neuropsychological research with patients with specific patterns of brain damage. As discovered with the

The basal ganglia, dopamine, and reward learning

Significant advances have been made in recent years into the functional neurophysiological, neurochemical, and neurocomputational characteristics of the basal ganglia and their dopaminergic inputs. Collectively, these studies suggest that dopamine neurons projecting to the basal ganglia are critical for learning to predict rewarding outcomes and acting to obtain them.

This idea arose from a series of pivotal studies that reported on recordings from dopamine neurons in monkeys and demonstrated a

An integrated view of the basal ganglia in learning

Theories regarding the role of dopamine in reward prediction have had a substantial impact on understanding the role of the basal ganglia in learning. They shed light on the basis for previous inconsistencies and highlight the neural mechanisms that bridge seemingly disparate findings. Integrating the domains of electrophysiology, neuroimaging, computational modeling, and neuropsychology has led to some general principles regarding the role of the basal ganglia in learning, as detailed below.

Interactions between the basal ganglia and other brain systems for learning

Neuropsychological and animal data, together with reinforcement learning models, have provided a detailed understanding of the circumstances under which the basal ganglia support learning and insights into the mechanisms by which they do so. Armed with this new understanding, there has been a renewed interest in understanding how this learning system is complemented by, and interacts with, other learning systems. These efforts have taken place in three main areas:

Conclusions and future directions

Volumes of research have highlighted the unique contributions of the basal ganglia and medial temporal lobes to learning and memory. However, some of the resulting characterizations, such as assigning implicit and explicit learning and memory to these systems, have turned out to be oversimplified. Moreover, a focus on assigning unique attributes to these two systems has overlooked the many ways in which these brain regions jointly contribute to behavior. Converging evidence from

Acknowledgments

We thank Suzanne Wood for comments on an earlier draft and members of the Learning Lab at Columbia University for helpful conversations about the research reviewed here. K.F. is supported by an NINDS NRSA training grant (F32 NS063632); D.S. is supported by a NARSAD Young Investigator Award, the Michael J Fox Foundation, and a National Science Foundation Early Career Award.

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