The neuroscience of remote memory

Recently, there has been renewed interest in the organization and neurobiology of remote memory, and the pace of work in this area has accelerated. Yet the recent literature does not suggest that a consensus is developing, and there is disagreement about both facts and their interpretation. This article undertakes a comprehensive review of the three kinds of evidence that have been most prominent in recent discussion: studies of retrograde amnesia in memory-impaired patients who have well-characterized lesions, neuroimaging of healthy volunteers, and work with experimental animals including lesion studies, imaging and mouse genetics. The available evidence tells a coherent story and leads to some straightforward conclusions about the neuroscience of remote memory.     

The cognitive neuroscience of memory distortion

Memory distortion occurs in the laboratory and in everyday life. This article focuses on false recognition, a common type of memory distortion in which individuals incorrectly claim to have encountered a novel object or event. By considering evidence from neuropsychology, neuroimaging, and electrophysiology, we address three questions. (1) Are there patterns of neural activity that can distinguish between true and false recognition? (2) Which brain regions contribute to false recognition? (3) Which brain regions play a role in monitoring or reducing false recognition? Neuroimaging and electrophysiological studies suggest that sensory activity is greater for true recognition compared to false recognition. Neuropsychological and neuroimaging results indicate that the hippocampus and several cortical regions contribute to false recognition. Evidence from neuropsychology, neuroimaging, and electrophysiology implicates the prefrontal cortex in retrieval monitoring that can limit the rate of false recognition.     

The human hippocampus and spatial and episodic memory

Finding one's way around an environment and remembering the events that occur within it are crucial cognitive abilities that have been linked to the hippocampus and medial temporal lobes. Our review of neuropsychological, behavioral, and neuroimaging studies of human hippocampal involvement in spatial memory concentrates on three important concepts in this field: spatial frameworks, dimensionality, and orientation and self-motion. We also compare variation in hippocampal structure and function across and within species. We discuss how its spatial role relates to its accepted role in episodic memory. Five related studies use virtual reality to examine these two types of memory in ecologically valid situations. While processing of spatial scenes involves the parahippocampus, the right hippocampus appears particularly involved in memory for locations within an environment, with the left hippocampus more involved in context-dependent episodic or autobiographical memory.     

A unified model of spatial and episodic memory

Medial temporal lobe structures including the hippocampus are implicated by separate investigations in both episodic memory and spatial function. We show that a single recurrent attractor network can store both the discrete memories that characterize episodic memory and the continuous representations that characterize physical space. Combining both types of representation in a single network is actually necessary if objects and where they are located in space must be stored. We thus show that episodic memory and spatial theories of medial temporal lobe function can be combined in a unified model.     

The cognitive neuroscience of memory: perspectives from neuroimaging research.

Cognitive neuroscience approaches to memory attempt to elucidate the brain processes and systems that are involved in different forms of memory and learning. This paper examines recent research from brain-damaged patients and neuroimaging studies that bears on the distinction between explicit and implicit forms of memory. Explicit memory refers to conscious recollection of previous experiences, whereas implicit memory refers to the non-conscious effects of past experiences on subsequent performance and behaviour. Converging evidence suggests that an implicit form of memory known as priming is associated with changes in posterior cortical regions that are involved in perceptual processing; some of the same regions may contribute to explicit memory. The hippocampal formation and prefrontal cortex also play important roles in explicit memory. Evidence is presented from recent PET scanning studies that suggests that frontal regions are associated with intentional strategic efforts to retrieve recent experiences, whereas the hippocampal formation is associated with some aspect of the actual recollection of an event.     

The cognitive neuroscience of constructive memory: remembering the past and imagining the future

Episodic memory is widely conceived as a fundamentally constructive, rather than reproductive, process that is prone to various kinds of errors and illusions. With a view towards examining the functions served by a constructive episodic memory system, we consider recent neuropsychological and neuroimaging studies indicating that some types of memory distortions reflect the operation of adaptive processes. An important function of a constructive episodic memory is to allow individuals to simulate or imagine future episodes, happenings and scenarios. Since the future is not an exact repetition of the past, simulation of future episodes requires a system that can draw on the past in a manner that flexibly extracts and recombines elements of previous experiences. Consistent with this constructive episodic simulation hypothesis, we consider cognitive, neuropsychological and neuroimaging evidence showing that there is considerable overlap in the psychological and neural processes involved in remembering the past and imagining the future.     

The status of cognitive neuroscience.

Cognitive neuroscience rests on findings, methods, and theory from three fields: experimental psychology, systems-level neuroscience, and computer science. The strong trend over the past few years has been for a greater integration across these fields. The influence of this interdisciplinary approach on current research on memory, perception, and language will be illustrated.     

The cognitive neuroscience of visual attention.

In current conceptualizations of visual attention, selection takes place through integrated competition between recurrently connected visual processing networks. Selection, which facilitates the emergence of a 'winner' from among many potential targets, can be associated with particular spatial locations or object properties, and it can be modulated by both stimulus-driven and goal-driven factors. Recent neurobiological data support this account, revealing the activation of striate and extrastriate brain regions during conditions of competition. In addition, parietal and temporal cortices play a role in selection, biasing the ultimate outcome of the competition.     

The cognitive neuroscience of sleep: neuronal systems,consciousness and learning

Sleep can be addressed across the entire hierarchy of biological organization. We discuss neuronal-network and regional forebrain activity during sleep, and its consequences for consciousness and cognition. Complex interactions in thalamocortical circuits maintain the electroencephalographic oscillations of non-rapid eye movement (NREM) sleep. Functional neuroimaging affords views of the human brain in both NREM and REM sleep, and has informed new concepts of the neural basis of dreaming during REM sleep -- a state that is characterized by illogic, hallucinosis and emotionality compared with waking. Replay of waking neuronal activity during sleep in the rodent hippocampus and in functional images of human brains indicates possible roles for sleep in neuroplasticity. Different forms and stages of learning and memory might benefit from different stages of sleep and be subserved by different forebrain regions.     

Generalist genes and cognitive neuroscience

Multivariate genetic research suggests that a single set of genes affects most cognitive abilities and disabilities. This finding already has far-reaching implications for cognitive neuroscience, and will become even more revealing when this - presumably large - set of generalist genes is identified. Similar to other complex disorders and dimensions, molecular genetic research on cognitive abilities and disabilities is adopting genome-wide association strategies. These strategies involve very large samples to detect DNA associations of small effect size using microarrays that simultaneously assess hundreds of thousands of DNA markers. When this set of generalist genes is identified, it can be used to provide solid footholds in the climb towards a systems-level understanding of how genetically driven brain processes work together to affect diverse cognitive abilities and disabilities.     

Theories of episodic memory

Theories of episodic memory need to specify the encoding (representing), storage, and retrieval processes that underlie this form of memory and indicate the brain regions that mediate these processes and how they do so. Representation and re-representation (retrieval) of the spatiotemporally linked series of scenes, which constitute an episode, are probably mediated primarily by those parts of the posterior neocortex that process perceptual and semantic information. However, some role of the frontal neocortex and medial temporal lobes in representing aspects of context and high-level visual object information at encoding and retrieval cannot currently be excluded. Nevertheless, it is widely believed that the frontal neocortex is mainly involved in coordinating episodic encoding and retrieval and that the medial temporal lobes store aspects of episodic information. Establishing where storage is located is very difficult and disagreement remains about the role of the posterior neocortex in episodic memory storage. One view is that this region stores all aspects of episodic memory ab initio for as long as memory lasts. This is compatible with evidence that the amygdala, basal forebrain, and midbrain modulate neocortical storage. Another view is that the posterior neocortex only gradually develops the ability to store some aspects of episodic information as a function of rehearsal over time and that this information is initially stored by the medial temporal lobes. A third view is that the posterior neocortex never stores these aspects of episodic information because the medial temporal lobes store them for as long as memory lasts in an increasingly redundant fashion. The last two views both postulate that the medial temporal lobes initially store contextual markers that serve to cohere featural information stored in the neocortex. Lesion and functional neuroimaging evidence still does not clearly distinguish between these views. Whether the feeling that an episodic memory is familiar depends on retrieving an association between a retrieved episode and this feeling, or by an attribution triggered by a priming process, is unclear. Evidence about whether the hippocampus and medial temporal lobe cortices play different roles in episodic memory is conflicting. Identifying similarities and differences between episodic memory and both semantic memory and priming will require careful componential analysis of episodic memory.     

Recurrent loops: Incorporating prediction error and semantic/episodic theories into Drosophila associative memory models

In 2003, Martin Heisenberg et al. presented a model of how associative memories could be encoded and stored in the insect brain. This model was extremely influential in the Drosophila memory field, but did not incorporate several important mammalian concepts, including ideas of separate episodic and semantic types of memory and prediction error hypotheses. In addition, at that time, the concept of memory traces recurrently entering and exiting the mushroom bodies, brain areas where associative memories are formed and stored, was unknown. In this review, I present a simple updated model incorporating these ideas, which may be useful for future studies.     

The neurodynamic bases of imitating learning and episodic memory

In this review, three essentially important processes in the development of cognitive behavior are considered, viz., knowledge of a spatial environment by means of physical activity, coding, and the calling of the existential context of episodic memory and imitation learning based on the mirror neural mechanism. The data show that the parietal and frontal systems, which are involved in learning by imitation, allow a developing animal to obtain skills of management and motive synergies in perisomatic space, as well as to understand the intentions and the purposes of the observed actions of other individuals. At the same time the widely distributed parietal and frontal and entorhinal–hippocampal system mediates spatial knowledge and the solution of the navigation tasks that are important for the creation of the existential context of episodic memory.     

Cognitive neuroscience of emotional memory

Emotional events often attain a privileged status in memory. Cognitive neuroscientists have begun to elucidate the psychological and neural mechanisms underlying emotional retention advantages in the human brain. The amygdala is a brain structure that directly mediates aspects of emotional learning and facilitates memory operations in other regions, including the hippocampus and prefrontal cortex. Emotion-memory interactions occur at various stages of information processing, from the initial encoding and consolidation of memory traces to their long-term retrieval. Recent advances are revealing new insights into the reactivation of latent emotional associations and the recollection of personal episodes from the remote past.