Learning

Learning is mediated by multiple memory systems in the brain, each of which involves a distinct anatomical pathway and supports a particular form of memory representation. The major aim of research on memory systems is to identify and distinguish the different contributions of specific brain structures and pathways, usually by contrasting the effects of selective damage to specific brain areas. Another major strategy focuses on localizing brain areas that are activated, that is, whose neurons are activated during particular aspects of memory processing. Some of these studies use newly developed functional imaging techniques to view activation of brain areas in humans performing memory tests. Another approach seeks to characterize the cellular code for memory within the activity patterns of single nerve cells in animals, by asking how information is represented by the activity patterns within the circuits of different structures in the relevant brain systems.

Each of the brain's memory systems begins in the vast expanse of the cerebral cortex, specifically in the so-called cortical association areas (see Figure 1). These parts of the cerebral cortex provide major inputs to each of three main pathways of processing in subcortical areas related to distinct memory functions. One system mediates declarative memory, the memory for facts and events that can be brought to conscious recollection and can be expressed in a variety of ways outside the context of learning. This system involves connections from the cortical association areas to the hippocampus via the parahippocampal region. The main output of hippocampal and parahippocampal processing is back to the same cortical areas that provided inputs to the hippocampus, and are viewed as the long-term repository of declarative memories.

The other two main pathways involve cortical inputs to specific subcortical targets that send direct outputs that control behavior. One of these systems mediates emotional memory, the attachment of affiliations and aversions towards otherwise arbitrary stimuli and modulation of the strength of memories that involve emotional arousal. This system involves cortical (as well as subcortical) inputs to the amygdala as the nodal stage in the association of sensory inputs to emotional outputs effected via the hypothalamic-pituitary axis and autonomic nervous system, as well as emotional influences over widespread brain areas. The second of these systems mediates procedural memory, the capacity to acquire habitual behavioral routines that can be performed without conscious control. This system involves cortical inputs to the striatum as a nodal stage in the association of sensory and motor cortical information with voluntary responses via the brainstem motor system. An additional, parallel pathway that mediates different aspects of sensori-motor adaptations involves sensory and motor systems pathways through the cerebellum.

The Declarative Memory System

Declarative memory is the "everyday" form of memory that most consider when they think of memory. Therefore, the remainder of this discussion will focus on the declarative memory system. Declarative memory is defined as a composite of episodic memory, the ability to recollect personal experiences, and semantic memory, the synthesis of the many episodic memories into the knowledge about the world. In addition, declarative memory supports the capacity for conscious recall and the flexible expression of memories, one's ability to search networks of episodic and semantic memories and to use this capacity to solve many problems.

Each of the major components of the declarative memory system contributes differently to declarative memory, although interactions between these areas are also essential. Initially, perceptual information as well as information about one's behavior is processed in many dedicated neocortical areas. While the entire cerebral cortex is involved in memory processing, the chief brain area that controls this processing is the prefrontal cortex. The processing accomplished by the prefrontal cortex includes the acquisition of complex cognitive rules and concepts and working memory, the capacity to store information briefly while manipulating or rehearsing the information under conscious control. In addition, the areas of the cortex also contribute critically to memory processing. Association areas in the prefrontal, temporal, and parietal cortex play a central role in cognition and in both the perception of sensory information and in maintenance of short-term traces of recently perceived stimuli. Furthermore, the organization of perceptual representations in cerebral cortical areas, and connections among these areas, are permanently modified by learning experiences, constituting the long term repository of memories.

The parahippocampal region, which receives convergent inputs from the neocortical association areas and sends return projections to all of these areas, appears to mediate the extended persistence of these cortical representations. Through interactions between these areas, processing within the cortex can take advantage of lasting parahippocampal representations, and so come to reflect complex associations between events that are processed separately in different cortical regions or occur sequentially in the same or different areas.

These individual contributions and their inter-actions are not conceived as sufficient to link representations of events to form episodic memories or to form generalizations across memories to create a semantic memory network. Such an organization requires the capacity to rapidly encode a sequence of events that make up an episodic memory, to retrieve that memory by re-experiencing one facet of the event, and to link the ongoing experience to stored episodic representations, forming the semantic network. The neuronal elements of the hippocampus contain the fundamental coding properties that can support this kind of organization.

However, interactions among the components of the system are undoubtedly critical. It is unlikely that the hippocampus has the storage capacity to contain all of one's episodic memories and the hippocampus is not the final storage site. Therefore, it seems likely that the hippocampal neurons are involved in mediating the reestablishment of detailed cortical representations, rather than storing the details themselves. Repetitive interactions between the cortex and hippocampus, with the parahippocampal region as intermediary, serve to sufficiently coactivate widespread cortical areas so that they eventually develop linkages between detailed memories without hippocampal mediation. In this way, the networking provided by the hippocampus underlies its role in the organization of the permanent memory networks in the cerebral cortex.

FIGURE 1