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This part presents four chapters on the concept of memory systems. The first considers the biology of memory systems. The second discusses multiple memory systems in the brain. The third presents a synthetic framework for characterizing memory subsystems. The fourth presents a synthesis of the chapters in this part.

Several ideas have been advanced about how memory is stored in the brain: by specific molecules, by a separate warehouse, by a switchboard that connects associations, and in terms of molecular and cellular plasticity. This book rejects all of these views as incorrect or simplistic, and introduces two major themes that govern the nature and organization of memory in the brain: (1) Memory is a fundamental property of brain, and its storage is intimately tied to ongoing information processing in the brain; (2) Memory is manifested in multiple ways by multiple, functionally, and anatomically distinct brain systems. This book adopts the view that conscious and unconscious forms of memory are distinct, and that the properties of each of these forms of memory are derived from the anatomy and physiological characteristics of the circuitry involved in each system.

This chapter contends that there are no logical conflicts between process views and system views of memory and that the two complement each other. The real controversy, however, lies in the existence of unitary versus multiple long-term memory systems. Three main parts constitute this chapter. The first one explores the differences between process-oriented versus systems-oriented approaches to the study of memory and explains why the two cannot be in conflict. The second provides a description and illustration of the differences between unitary versus multiple memory theories and shows why they are necessarily in conflict. The last part demonstrates several critical empirical findings that converted the author of this chapter from a unitarian believer to a multiple memory systems enthusiast. The chapter concludes with a prediction that the future belongs to the multiple memory systems framework.

This chapter presents substantial direct evidence for the existence and initial localization of multiple memory systems in the brain. Multiple dissociation studies show that in rats the hippocampal region mediates memory for adoption of the ‘place’ strategy in a T-maze and expression of episodic memories; in humans this region mediates memory for facts and events. The striatum plays a critical role in the learning of habitual behavioural responses, as reflected in rats by the ‘response’ strategy in a T-maze and stimulus-approach learning in the radial maze, and in humans by probabilistic learning of cue-response associations. These studies have also provided compelling evidence that the amygdala is critical to emotional learning, as reflected in the acquisition of cue preferences in rats and conditioned emotional responses in humans. Across all these experiments, a salient theme is that even for identical learning materials, different forms of memory are mediated largely independently and in parallel.

This chapter examines neuropsychological and non-human animal findings and discusses ways in which neuroimaging research has advanced our understanding of memory systems in the human brain. It focuses on the question of whether brain-imaging data can decide between unitary vs. multiple memory systems, i.e. whether information is stored, consolidated, and retrieved always within one and the same biological substrate or whether distinct systems are involved depending on the type of material or task.

Learning, and hence memory, is ubiquitous not only throughout the animal kingdom, but apparently throughout many regions of the brain. Is all learning reducible to a single common form? Neuropsychological dissociations suggest that the mammalian brain possesses a number of different and potentially independent memory systems, with different mechanisms and anatomical dispositions, some of which are neurally widely dispersed and others of which are narrowly organized. Among the types considered are: short-term memory; knowledge and skills; stable associative memory; event memory; and priming. As double or multiple dissociations do not lead to logically inevitable conclusions, it has been argued that an alternative to multiple memory systems is variable modes of processing. Multiple memory systems may possibly share some common cellular mechanisms, but such mechanisms do not define the separate properties at the systems level.

An account of multiple memory systems in terms of functional dissociations within brain systems is presented in this chapter. Data from both the human and non-human literatures are considered. It focuses on five brain regions — hippocampus, amygdale, thalamus, prefrontal cortex, basal ganglia — that have been reliably identified with learning and memory processes. The aim is to show that, together, these regions comprise an array of integrated yet functionally dissociable neural circuits which is a critical aspect of learning and memory. It argues that memory should not be regarded as a unitary process, rather, it presents evidence that within the brain's complex organization, differentiated structures can be implicated in subserving specific components of learning and memory and that these functions can be dissociated using sensitive behavioural paradigms.

Multiple memory systems describes how memories can be declarative or non-declarative; incentive learning produces one type of non-declarative memory. Patients with bilateral hippocampal damage have declarative memory deficits (amnesia) but intact non-declarative memory; patients with striatal dysfunction, for example, Parkinson’s patients who lose striatal dopamine have impaired incentive learning but intact declarative memory. Rats with lesions of the fornix (hippocampal output pathway), but not lesions of the dorsal striatum, have impaired spatial (declarative) memory; rats with lesions of the dorsal striatum, but not fornix, have impaired stimulus–response memory that relies heavily on incentive learning. These memory systems possibly inhibit one another to control responding: in rats, a group that received fornix lesions and had impaired spatial learning did better on an incentive task; in humans, hippocampus damage was associated with improvement on an incentive learning task and striatal damage was associated with increased involvement of the hippocampus in a route-recognition task.

Five themes of importance for understanding memory run through this chapter and it recognizes that that emotional memories are not the only kinds of memories that can be stored in the mammalian brain. Paul Gold's hypothesis suggests that the content of a memory, including its emotional content, may determine how and in what part of the brain it is stored. This concept is central to current thinking about multiple memory systems. Representations of the properties of stimuli and events that make up any learning situation become the content of the memories that are stored in the brain. One of the properties of such stimuli and events, often called reinforcers, is the affective states these stimuli and events produce in the organisms that come into contact with them. Two experiments illustrate the difference between the affective and memory-improving properties of reinforcers.

The model of enduring change in psychotherapy featuring memory reconsolidation and emotional arousal was based on recent neuroscientific advances that were presented originally from a predominantly psychological perspective. This chapter translates the components and processes of the model into evidence-based neural systems terms. This neural circuitry model highlights what is known and not known and where new research is most urgently needed. The authors then consider the research agenda, emphasizing what they consider to be the most important knowledge gaps. The basic science research agenda focuses on a variety of topics pertaining to memory and memory reconsolidation as well as interactions between emotion and memory. The clinical science research agenda focuses on the most pressing issues pertaining to the processes and mechanisms contributing to enduring change in psychotherapy. The potential exists to develop a new taxonomy of clinical interventions based on what problems are being targeted, how intractable they are, and how long-lasting the intervention needs to be.

Visual imprinting leads to changes in a nervous system that may not have been marked by previous visual experience, and so encourages the hope of discovering the neural bases of the learning process. The intermediate and medial part of the hyperstriatum ventrale, a sheet of cells within the cerebral hemispheres, plays a crucial role in visual imprinting, particularly in the memory process of recognition. The cellular and sub-cellular changes that take place in this part of the hyperstriatum ventrale after imprinting are described. The right and left hyperstriatum ventrale regions play different roles in the imprinting process, and evidence is given for the existence of multiple memory systems in the chick brain.

Among many mammalian innovations, a new type of cortex emerged: the neocortex. According to our proposal, part of the neocortex housed what we call the biased-competition memory system. It uses specialized representations, stored in the agranular prefrontal cortex, to regulate energy economics by generating several top-down biases: (1) among neural representations that compete to control behavior; (2) toward high-energy foraging when warranted by yet higher energy expectations; and (3) toward patient or urgent foraging, depending on conditions and individual tendencies. Examples of competing representations include outcome-directed behaviors versus habits, Pavlovian versus instrumental memories, navigation in extrinsic versus intrinsic coordinates, fragile associations versus strong ones, and the use of current versus obsolete contexts for making foraging choices. By learning which kind of representations should prevail over others and biasing behavioral control toward them, early mammals could adapt to resource fluctuations more effectively than their ancestors could.