Lost forever or temporarily misplaced? The long debate about the nature of memory impairment

Studies of memory impairment in humans and experimental animals have been fundamental to learning about the organization of memory and its cellular and molecular substrates. When memory impairment occurs, especially after perturbations of the nervous system, the question inevitably arises whether the impairment reflects impaired information storage or impaired accessibility. This topic has been the subject of considerable commentary and experimental work over the years. In this reappraisal, I first consider four broad areas of behavioral study from the 1970s and 1980s that led to a dominant and compelling view of memory impairment as a deficit of information storage. Second, I identify some ambiguities that arise about how the terms "storage" and "retrieval" are applied, especially when the evidence is somewhat indirect and based on a behavioral-psychological level of analysis. I then review neurobiological findings that have been largely overlooked in these discussions. The relevant studies are ones where it has been possible to monitor neurons and synapses in direct relation to behavioral memory, for example, in animals with simple nervous systems and in single cell recordings from behaving monkeys. This work provides a straightforward and illuminating perspective on the question and confirms the view that first emerged from less direct evidence.     

Dissociating Long-term Memory Systems: Comment on Nyberg and Tulving (1996)

Nyberg and Tulving (1996) presented functional, developmental, psychopharmacological and neuropsychological evidence for each possible pairwise dissociation between episodic, semantic, procedural and PRS memory systems and concluded that these systems are therefore independent. I argue that this exercise is questionable on a number of grounds, and consider in detail the evidence that Nyberg and Tulving cite in favour of one particular dissociation, that between episodic and procedural memory. I suggest that a truer interpretation of the evidence is that these types of memory are closely linked, and that the multiple memory systems view fails to account for a variety of findings.     

The relation between verbal and visuospatial memory and autobiographical memory

The basic-systems approach (Rubin, 2005, 2006) states that autobiographical memory is supported by other cognitive systems and argues that autobiographical memories are constructed from interactions between cognitive systems, such as language, vision and emotion. Although deficiencies in one or more of the basic systems influence the properties of autobiographical memories, little is known about how these cognitive abilities and autobiographical memory are related. To assert whether participants with stronger cognitive abilities also perform better on autobiographical memory tests, participants who completed verbal and visuospatial memory tests also recorded one personal event, which they recalled after a certain interval. Participants who performed well on the verbal memory tests also had better retention for the personal event, providing support for the basic-systems approach to autobiographical memory and preliminary support for the view that people have more memories from adolescence and early adulthood because the memory system works optimally in these lifetime periods.     

A cognitive neuroscience account of posttraumatic stress disorder and its treatment

Recent research in the areas of animal conditioning, the neural systems underlying emotion and memory, and the effect of fear on these systems is reviewed. This evidence points to an important distinction between hippocampally-dependent and non-hippocampally-dependent forms of memory that are differentially affected by extreme stress. The cognitive science perspective is related to a recent model of posttraumatic stress disorder, dual representation theory, that also posits separate memory systems underlying vivid reexperiencing versus ordinary autobiographical memories of trauma. This view is compared with other accounts in the literature of traumatic memory processes in PTSD, and the contrasting implications for therapy are discussed.     

A unitary signal-detection model of implicit and explicit memory

Do dissociations imply independent systems? In the memory field, the view that there are independent implicit and explicit memory systems has been predominantly supported by dissociation evidence. Here, we argue that many of these dissociations do not necessarily imply distinct memory systems. We review recent work with a single-system computational model that extends signal-detection theory (SDT) to implicit memory. SDT has had a major influence on research in a variety of domains. The current work shows that it can be broadened even further in its range of application. Indeed, the single-system model that we present does surprisingly well in accounting for some key dissociations that have been taken as evidence for independent implicit and explicit memory systems.     

Acetylcholine modulation of neural systems involved in learning and memory

Extensive evidence supports the view that cholinergic mechanisms modulate learning and memory formation. This paper reviews evidence for cholinergic regulation of multiple memory systems, noting that manipulations of cholinergic functions in many neural systems can enhance or impair memory for tasks generally associated with those neural systems. While parallel memory systems can be identified by combining lesions with carefully crafted tasks, most—if not all—tasks require the combinatorial participation of multiple neural systems. This paper offers the hypothesis that the magnitude of acetylcholine (ACh) release in different neural systems may regulate the relative contributions of these systems to learning. Recent studies of ACh release, obtained with in vivo microdialysis samples during training, together with direct injections of cholinergic drugs into different neural systems, provide evidence that release of ACh is important in engaging these systems during learning, and that the extent to which the systems are engaged is associated with individual differences in learning and memory.     

The Relations of Visuo-Motor Conflict to Personality Traits and Cardio-Vascular Activity

This paper presents a review and critical analysis of some research findings and conclusions which seem to demonstrate that picture recognition memory is superior to verbal recognition memory. It cautions against accepting these data as evidence for two (picture-verbal) memory systems. Several alternative explanations of the picture-verbal performance discrepancy are derived from interference theory and partial learning theory. “Picture” as a stimulus category is vague and overinclusive. Recognition memory capacity varies from poor to excellent depending on the “pictures,” a fact not in harmony with a memory model employing a unitary processing mechanism for pictorial stimuli. Perceptual constancy is invoked in support of a view that is antagonistic to the implication that the human recognition memory mechanism is error free.     

Working memory retention systems: a state of activated long-term memory

High temporal resolution event-related brain potential and electroencephalographic coherence studies of the neural substrate of short-term storage in working memory indicate that the sustained coactivation of both prefrontal cortex and the posterior cortical systems that participate in the initial perception and comprehension of the retained information are involved in its storage. These studies further show that short-term storage mechanisms involve an increase in neural synchrony between prefrontal cortex and posterior cortex and the enhanced activation of long-term memory representations of material held in short-term memory. This activation begins during the encoding/comprehension phase and evidently is prolonged into the retention phase by attentional drive from prefrontal cortex control systems. A parsimonious interpretation of these findings is that the long-term memory systems associated with the posterior cortical processors provide the necessary representational basis for working memory, with the property of short-term memory decay being primarily due to the posterior system. In this view, there is no reason to posit specialized neural systems whose functions are limited to those of short-term storage buffers. Prefrontal cortex provides the attentional pointer system for maintaining activation in the appropriate posterior processing systems. Short-term memory capacity and phenomena such as displacement of information in short-term memory are determined by limitations on the number of pointers that can be sustained by the prefrontal control systems.     

Multiple memory systems: the power of interactions

Two relatively simple theories of brain function will be used to demonstrate the explanatory power of multiple memory systems in your brain interacting cooperatively or competitively to directly or indirectly influence cognition and behaviour. The view put forth in this mini-review is that interactions between memory systems produce normal and abnormal manifestations of behaviour, and by logical extension, an understanding of these complex interactions holds the key to understanding debilitating brain and psychiatric disorders.     

Why faces are and are not special: an effect of expertise

Recognition memory for faces is hampered much more by inverted presentation than is memory for any other material so far examined. The present study demonstrates that faces are not unique with regard to this vulnerability to inversion. The experiments also attempt to isolate the source of the inversion effect. In one experiment, use of stimuli (landscapes) in which spatial relations among elements are potentially important distinguishing features is shown not to guarantee a large inversion effect. Two additional experiments show that for dog experts sufficiently knowledgeable to individuate dogs of the same breed, memory for photographs of dogs of that breed is as disrupted by inversion as is face recognition. A final experiment indicates that the effect of orientation on memory for faces does not depend on inability to identify single features of these stimuli upside down. These experiments are consistent with the view that experts represent items in memory in terms of distinguishing features of a different kind than do novices. Speculations as to the type of feature used and neuropsychological and developmental implications of this accomplishment are offered.     

Associative memory and the medial temporal lobes

Associative recognition and recall depend on structures in the medial temporal lobes (MTLs). There is disagreement about whether associative memory is functionally heterogeneous, whether it is functionally distinct from intra-item associative memory and how the MTLs contribute to this kind of memory. Despite an increase in research on associative memory, work has lacked a theoretical framework to guide design and interpretation of studies. One view provides a useful framework by postulating that associative memories differ in the degree to which their informational components converge in MTL structures that create familiarity-supporting or recollection-supporting memory representations. Using this framework, we consider psychological, lesion and functional imaging evidence, highlighting how informational convergence in the brain underlies the associative nature of both memory and perception.     

How fuzzy-trace theory predicts true and false memories for words,sentences, and narratives

Fuzzy-trace theory posits independent verbatim and gist memory processes, a distinction that has implications for such applied topics as eyewitness testimony. This distinction between precise, literal verbatim memory and meaning-based, intuitive gist accounts for memory paradoxes including dissociations between true and false memory, false memories outlasting true memories, and developmental increases in false memory. We provide an overview of fuzzy-trace theory, and, using mathematical modeling, also present results demonstrating verbatim and gist memory in true and false recognition of narrative sentences and inferences. Results supported fuzzy-trace theory's dual-process view of memory: verbatim memory was relied on to reject meaning-consistent, but unpresented, sentences (via recollection rejection). However, verbatim memory was often not retrieved, and gist memory supported acceptance of these sentences (via similarity judgment and phantom recollection). Thus, mathematical models of words can be extended to explain memory for complex stimuli, such as narratives, the kind of memory interrogated in law.     

An analysis of independence and interactions of brain substrates that subserve multiple attributes, memory systems, and underlying processes

It is proposed that memory is organized into event-based, knowledge-based, and rule-based memory systems. Furthermore, each system is composed of the same set of multiple attributes and characterized by a set of process oriented operating characteristics that are mapped onto multiple neural regions and interconnected neural circuits. Based on this theoretical model of memory, it is possible to investigate the independence and interaction among brain regions between any two systems for any of the proposed attributes or processes. This applies also to the investigation of independence and interactions between any two attributes within a system and between processes associated with a system for any of the proposed attributes. In this article, research evidence is presented to suggest that there are both dissociations and interactions between the hippocampus and caudate nucleus in mediating spatial and response attributes within the event-based memory system, between the hippocampus and the parietal cortex in subserving the spatial attribute within the event-based and knowledge-based memory systems, and between the hippocampus and the prefrontal cortex in subserving the spatial attribute within the event-based and rule-based memory systems.     

Decisions and the evolution of memory: multiple systems, multiple functions

Memory evolved to supply useful, timely information to the organism's decision-making systems. Therefore, decision rules, multiple memory systems, and the search engines that link them should have coevolved to mesh in a coadapted, functionally interlocking way. This adaptationist perspective suggested the scope hypothesis: When a generalization is retrieved from semantic memory, episodic memories that are inconsistent with it should be retrieved in tandem to place boundary conditions on the scope of the generalization. Using a priming paradigm and a decision task involving person memory, the authors tested and confirmed this hypothesis. The results support the view that priming is an evolved adaptation. They further show that dissociations between memory systems are not--and should not be--absolute: Independence exists for some tasks but not others.     

Recognition memory and awareness: An experiential approach

Abstract

This article reviews recent studies that have adopted an experiential approach to recognition memory and awareness. This approach measures two subjective states of awareness in recognition memory, remembering (or conscious recollection) and knowing (or familiarity). There is now evidence of quite a few experimental dissociations between these two states of awareness. These dissociations impose additional constraints on theories about relations between awareness and memory systems or processes.     

Lateral and anterior thalamic lesions impair independent memory systems

Damage to the medial region of the thalamus, both in clinical cases (e.g., patients with infarcts or the Korsakoff's syndrome) and animal lesion models, is associated with variable amnesic deficits. Some studies suggest that many of these memory deficits rely on the presence of lateral thalamic lesions (LT) that include the intralaminar nuclei, presumably by altering normal function between the striatum and frontal cortex. Other studies suggest that the anterior thalamic nuclei (AT) may be more critical, as a result of disruption to an extended hippocampal system. Here, highly selective LT and AT lesions were made to test the prediction that these two regions contribute to two different memory systems. Only LT lesions produced deficits on a preoperatively acquired response-related (egocentric) working memory task, tested in a cross-maze. Conversely, only AT lesions impaired postoperative acquisition of spatial working memory, tested in a radial maze. These findings provide the first direct evidence of a double dissociation between the LT and AT neural aggregates. As the lateral and the anterior medial thalamus influence parallel independent memory processing systems, they may each contribute to memory deficits, depending on lesion extent in clinical and experimental cases of thalamic amnesia.     

Behavioural evidence for separating components within visuo-spatial working memory

Several different sources of evidence support the idea that visuo-spatial working memory can be segregated into separate cognitive subsystems. However, the nature of these systems remains unclear. Recently we reported data from neurological patients suggesting that information about visual appearance is retained in a different subsystem from information about spatial location. In this paper we report latency data from neurologically intact participants showing an experimental double dissociation between memory for appearance and memory for location. This was achieved by use of a selective dual task interference technique. This pattern provides evidence supporting the segregation of visuo-spatial memory between two systems, one of which supports memory for stimulus appearance and the other which supports memory for spatial location.     

Somatic and autonomic indexes of recovery from electroconvulsive shock-induced amnesia in rats

Autonomic response indexes of experimental amnesia have recently been found to have higher electroconvulsive shock (ECS) intensity thresholds and steeper retrograde gradients than have traditional somatic indexes. The present studies examined the hypothesis that recovery from somatically indexed experimental amnesia depends upon the existence of autonomically available residual memory. In a between-subjects design, a 200-mA ECS was used to produce amnesia for a tone-footshock pairing as indicated by lick suppression, defection, and bradycardia. The next day, these amnesic animals received a reminder footshock outside of the training apparatus, which was found to restore memory on a test trial 24 hr later. The behavior of control groups indicated that this reminder effect was due to the restoration of specific memory rather than systemic consequences of treatment. With a within-subjects design, a second experiment obtained a reminder effect in animals individually shown to be "fully" amnesic by all three response indexes monitored. A third experiment varied the intensity of the reminder footshock and revealed that the different memory indexes examined do not have reminder-footshock thresholds inversely related to their initial resistance to amnesia. The results support a retrieval-failure view of experimental amnesia and suggest that the same fundamental physiological processes underlie both autonomically indexed memory and somatically indexed memory.