Separate Memory Systems Research Articles

Neuropsychology of Learning and Memory in Teleost Fish

Traditionally, brain and behavior evolution was viewed as an anagenetic process that occurred in successive stages of increasing complexity and advancement. Fishes, considered the most primitive vertebrates, were supposed to have a scarcely differentiated telencephalon, and limited learning capabilities. However, recent developmental, neuroanatomical, and functional data indicate that the evolution of brain and behavior may have been more conservative than previously thought. Experimental data suggest that the properties and neural basis of learning and memory are notably similar among teleost fish and land vertebrates. For example, lesion studies show that the teleost cerebellum is essential in classical conditioning of discrete motor responses. The lateral telencephalic pallium of the teleost fish, proposed as homologous to the hippocampus, is selectively involved in spatial learning and memory, and in trace classical conditioning. In contrast, the medial pallium, considered homologous to the amygdala, is involved in emotional conditioning in teleost fish. The data reviewed here show a remarkable parallelism between mammals and teleost fish concerning the role of different brain centers in learning and memory and cognitive processes. These evidences suggest that these separate memory systems could have appeared early during the evolution of vertebrates, having been conserved through phylogenesis.

Which Memory Processes are Affected in Patients With Obstructive Sleep Apnea? An Evaluation of 3 Types of Memory

To investigate which memory processes are affected by obstructive sleep apnea (OSA). Three separate memory systems were investigated in patients with OSA and normal subjects. Verbal episodic memory was tested after forced encoding, in order to control the level of attention during item presentation; procedural memory was tested using a simplified version of a standard test with an interfering task; lastly, working memory was examined with validated paradigms based on a theoretical model. Sleep laboratory and outpatient sleep clinic in a French tertiary-care university hospital. Ninety-five patients with OSA and 95 control subjects matched for age and level of education. Group 1 (54 patients, 54 controls) underwent an extensive battery of tasks evaluating verbal episodic, procedural, and working memory. Group 2 (16 patients, 16 controls) underwent procedural memory tests only, and group 3 (25 patients, 25 controls) working memory tests only. N/A. Compared with matched controls, patients with OSA exhibited a retrieval deficit of episodic memory but intact maintenance, recognition, and forgetfulness; decreased overall performance in procedural memory, although pattern learning did occur; and impairment of specific working memory capabilities despite normal short-term memory. No consistent correlation was found between OSA severity and memory deficit. The long duration of the test session did not negatively impact the patients' performance. Memory impairment in OSA is mild and does not affect all memory processes but, rather, specific aspects, underscoring the need for extensive and specific memory testing in clinical and research settings.

Dissociable memory effects after medial thalamus lesions in the rat

Variable neuropathology in cases of diencephalic amnesia has led to uncertainty in identifying key thalamic nuclei and their potential role in learning and memory. Based on the principal neural connections of the medial thalamus, the current study tested the hypothesis that different aggregates of thalamic nuclei contribute to separate memory systems. Lesions of the anterior thalamic aggregate (AT), which comprises the anterodorsal, anteromedial and anteroventral nuclei produced substantial deficits in both working and reference spatial memory in a radial arm maze task in rats, supporting the view that the AT is an integral part of a hippocampal memory system. Lesions to the lateral thalamic aggregate (LT), which comprises the intralaminar nuclei (centrolateral, paracentral and rostral central medial nuclei) and lateral mediodorsal thalamic nuclei (lateral and paralamellar nuclei) produced a mild working memory impairment only, while lesions to the posteromedial thalamic aggregate (MT), which comprises the central and medial mediodorsal thalamic nuclei and the intermediodorsal nucleus had no effect on radial arm maze performance. In contrast, only MT lesions impaired learning associated with memory for reward value, consistent with the idea that the MT contributes to an amygdala memory system. Compared with chance discrimination, the control and AT groups, but not MT or LT groups, showed evidence for temporal order memory for two recently presented objects; all groups showed intact object recognition for novel vs. familiar objects. These new dissociations show that different medial thalamic aggregates participate in multiple memory systems and reinforce the idea that memory deficits in diencephalic amnesics may vary as a function of the relative involvement of different thalamic regions.

Hallmarks of a common forebrain vertebrate plan: Specialized pallial areas for spatial, temporal and emotional memory in actinopterygian fish

In mammals and birds different pallial forebrain areas participate in separate memory systems. In particular, the hippocampal pallium is implicated in spatial memory and temporal attribute processing, whereas the amygdalar pallium is involved in emotional memory. Here we analyze the involvement of teleost fish lateral and medial pallia, proposed as homologous to the hippocampus and amygdala, respectively, in a variety of learning and memory tasks, such as spatial memory; reversal learning; delay or trace motor classical conditioning; heart rate, emotional classical conditioning; and two way active avoidance conditioning. Results show that the damage to the lateral pallium produces a profound deficit in spatial learning and memory in teleost fish. In addition, lateral pallium lesions produce a significant deficit in trace classical conditioning, whereas they have no significant effects on delay conditioning, or in heart rate conditioning. In contrast, medial pallium lesions disrupt emotional, heart rate conditioning and avoidance conditioning, but spare spatial memory and temporal stimulus processing. These data demonstrate a striking functional similarity between the medial and lateral pallia of teleost fish and the pallial amygdala and hippocampal pallium of land vertebrates, respectively. The reviewed evidence suggest that these two separate memory systems, the hippocampus-dependent spatial, relational or temporal memory system, and the amygdala based emotional memory system, could have appeared early during evolution, having conserved their functional identity through vertebrate phylogenesis.

Implicit and Explicit Memory in Children With Congenital and Acquired Brain Disorder.

Implicit and explicit memory were examined in 8- to 15-year-old children with myelomeningocele and shunted hydrocephalus, severe traumatic brain injuries, or orthopedic injuries. Each group included between 22 and 29 children. Children completed a fragmented picture identification task to assess perceptual priming and a semantic decision-making task to assess conceptual priming. Each task also assessed procedural learning as well as explicit recall and recognition. All 3 groups showed significant perceptual and semantic priming of similar magnitude. In contrast, both brain-disordered groups displayed poorer explicit memory than did the comparison group. No group showed significant procedural learning on either task. Age and IQ were stronger predictors of explicit recall than of implicit memory. The findings indicate that implicit memory is relatively intact in many children with congenital and acquired brain disorders, despite deficits in explicit memory, and support the existence of separate memory systems in children.

Anomalies in Cognition: Olfactory Memory

The two experiments presented in this paper examine the effects of strategies and interference tasks on odor recognition. In the first experiment (an extension of Lyman and McDaniel's study from 1986 ), participants were asked to smell 30 odors and to perform different elaborative tasks for each of them such as: (1) providing a name or a short definition; (2) creating an image; (3) describing a specific life episode; (4) simply smelling the odors. Results showed no effect of encoding tasks on the correct recognition of odors. In the second experiment, participants were exposed to either 15 olfactory stimuli, 15 visual stimuli (photographs of human faces), or 15 acoustic stimuli (environmental sounds). In the four sessions of the experiment, they had to recognize the stimuli whether in a no-interference condition, or in an intramodality, or in two intermodalities interfering conditions. Consistently with the literature, interference affects recognition for visual and acoustic material but has no effect on odor recognition. The results of both experiments and some other anomalies in olfactory memory are discussed and tentatively integrated into a single model. The main assumption is that memory for odors represents a unique and separate memory system.

Developmental patterns of verbal and visuospatial spans.

This study presents developmental data for verbal and spatial memory tasks: Corsi's block-tapping test and Luria's verbal learning test. Norms have been collected from 275 primary and early secondary school children aged from 5 years, 4 months to 13 years, 6 months. Our results confirm a slow and constant improvement in performances over time, and the advantage of about 1.5 items of the verbal span over the spatial span supports the existence of developmental differences between separate memory systems. No significant sex difference was found even if a slight trend in verbal span favouring female subjects is present.

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.

The Effect of Mental Practice on Performance in a Sequential Reaction Time Task

The effect of mental practice on performance in a dot-location RT task was investigated. Participants (N = 40) were required either to mentally practice, physically practice, or do no practice on an RT task in which the signals appeared in a repeating sequence. Correct mental practice, as opposed to incorrect mental practice and no practice, was predicted to have a positive (enhancing) effect on performance of the RT task. Despite previous evidence that mental rehearsal does enhance performance in many perceptual-motor tasks, neither correct nor incorrect mental rehearsal affected subsequent sequence learning; that is, no mental practice effect was observed. That surprising result is discussed in terms of motivational, psychoneuromuscular, separate memory systems, and transfer-appropriate processing explanations of mental practice.

Associating object names with descriptions of shape that distinguish possible from impossible objects

Five experiments examine the proposal that object names are closely linked to representations of global, 3D shape by comparing memory for simple line drawings of structurally possible and impossible novel objects. Objects were rendered impossible through local edge violations to global coherence (cf. Schacter, Cooper, & Delaney, 1990) and supplementary observations confirmed that the sets of possible and impossible objects were matched for their distinctiveness. Employing a test of explicit recognition memory, Experiment 1 confirmed that the possible and impossible objects were equally memorable. Experiments 2–4 demonstrated that adults learn names (single-syllable non-words presented as count nouns, e.g., “This is a dax”) for possible objects more easily than for impossible objects, and an item-based analysis showed that this effect was unrelated to either the memorability or the distinctiveness of the individual objects. Experiment 3 indicated that the effects of object possibility on name learning were long term (spanning at least 2 months), implying that the cognitive processes being revealed can support the learning of object names in everyday life. Experiment 5 demonstrated that hearing someone else name an object at presentation improves recognition memory for possible objects, but not for impossible objects. Taken together, the results indicate that object names are closely linked to the descriptions of global, 3D shape that can be derived for structurally possible objects but not for structurally impossible objects. In addition, the results challenge the view that object decision and explicit recognition necessarily draw on separate memory systems, with only the former being supported by these descriptions of global object shape. It seems that recognition also can be supported by these descriptions, provided the original encoding conditions encourage their derivation. Hearing an object named at encoding appears to be just such a condition. These observations are discussed in relation to the effects of naming in other visual tasks, and to the role of visual attention in object identification.

Multiple spatial learning strategies in goldfish (Carassius auratus)

There is a considerable amount of evidence that mammals and birds can use different spatial learning strategies based on multiple learning and memory systems. Unfortunately, only a few studies have investigated spatial learning and memory mechanisms in other vertebrates. This study aimed to identify the strategies used by goldfish to solve two different spatial tasks in a series of three experiments. In experiment 1, two groups of goldfish (Carassius auratus) were trained either in a spatial constancy task (SC), in which visual cues signalled the goal indirectly, or in a directly cued task (DC) in which similar cues signalled the goal directly. Transfer tests were conducted to study the effects of discrete cue deletion on the performance in both tasks. In these transfer tests the performance of the animals trained in the DC task dropped to chance level when the cue that signalled the goal directly was removed. In contrast, the removal of any single cue did not disrupt SC performance. In experiment 2, fish trained in the SC or the DC task were trained with the goal reversed. Goldfish in the SC group needed fewer sessions to master the reversal task than DC animals. Finally, experiment 3 investigated the effects of a substantial modification of the geometrical features of the apparatus on the performance of animals trained in the SC or in the DC condition. The performance of DC goldfish was not affected, whereas the same change disrupted performance in the SC animals despite the presence of the visual cues. These results suggest that there are separate spatial learning and memory systems in fish. Whereas the DC animals used a typical guidance strategy, relying only on the cue that signalled the goal directly, SC fish relied on a strategy with the properties of an actual spatial mapping system. Thus, the comparative approach points to the generality of these learning strategies among vertebrates.

The relationship between skill learning and repetition priming: Experimental and computational analyses.

Skill learning and repetition priming are considered by some to be supported by separate memory systems. The authors examined the relationship between skill learning and priming in 3 experiments using a digit entering task, in which participants were presented with unique and repeated 5-digit strings with controlled sequential structure. Both skill learning and priming were observed across a wide range of skill levels. Performance reflected the effects of learning at 3 different levels of stimulus structure, calling into question a binary dichotomy between item-specific priming and general skill learning. Two computational models were developed which demonstrated that previous dissociations between skill learning and priming can occur within a single memory system. The experimental and computational results are interpreted as suggesting that skill learning and priming should be viewed as 2 aspects of a single incremental learning mechanism.

The relationship between skill learning and repetition priming: experimental and computational analyses.

Skill learning and repetition priming are considered by some to be supported by separate memory systems. The authors examined the relationship between skill learning and priming in 3 experiments using a digit entering task, in which participants were presented with unique and repeated 5-digit strings with controlled sequential structure. Both skill learning and priming were observed across a wide range of skill levels. Performance reflected the effects of learning at 3 different levels of stimulus structure, calling into question a binary dichotomy between item-specific priming and general skill learning. Two computational models were developed which demonstrated that previous dissociations between skill learning and priming can occur within a single memory system. The experimental and computational results are interpreted as suggesting that skill learning and priming should be viewed as 2 aspects of a single incremental learning mechanism.

Perception and conception Separate memory systems in the medial temporal lobe

The purpose of the present study was to investigate, by using positron emission tomography, whether the functionally different types of information are subserved by different memory systems in human medial temporal lobe structures. Before explicit retrieval tests during scans, subjects studied words in perceptually and conceptually processed manners separately. It was found that different parts of the medial temporal lobe structures were involved in each of the different conditions. These results indicated that perceptually and conceptually processed types of information were subserved by at least two partially segregated memory systems in human medial temporal lobe structures.

What Differentiates Declarative and Procedural Memories: Reply to Cohen, Poldrack, and Eichenbaum (1997)

Cohen, Poldrack, and Eichenbaum (1997; hereafter CPE) offer an account of the nature of individual items in memory and how they relate to one another. They argue that there are two separate memory systems, procedural and declarative (Cohen & Eichenbaum, 1993; Cohen & Squire, 1980). These systems differ in their neuroanatomic substrates, in their operating characteristics, and in the nature of the representations they use. CPE argue that representations in the declarative memory system are compositional, meaning that declarative representations may be composed of other declarative representations. Declarative memories are also flexible, meaning they can be accessed in contexts that differ from those in which they were encoded. Procedural memories, on the other hand, are neither compositional nor flexible. I will argue that there is not sufficient reason to argue that procedural and declarative memories have these distinct characteristics. Both procedural and declarative memories are arguably compositional, and both can appear flexible or inflexible, depending on testing conditions.

Searching for Memory Systems

In his comment on Nyberg and Tulving's (1996) article, Shanks (this issue) argues that the dissociation evidence we presented for the multiple memory systems approach is weak. In this reply, we consider his comments, discuss some inconsistencies in his arguments, and note that he seems to have overlooked some of our points. We maintain our position that dissociation evidence constitutes one important source of support for separate memory systems, and we argue that converging evidence from dissociation studies and functional neuroimaging studies strongly indicates the existence of multiple human memory systems.

A comparison of forgetting in an implicit and explicit memory task.

Among possible criteria for distinguishing separate memory systems for implicit and explicit memory is that of substantial differences in either the form or rate of forgetting. Prior literature has claimed both differential forgetting and equivalent forgetting for implicit and explicit tasks. Existing experimental data for word-stem completion and explicit control tasks were reviewed and shown to be inconclusive. Our experiments measure forgetting in comparable implicit and explicit memory tasks of stem completion and stem cued recall. The form and the rate of forgetting are essentially the same for these implicit and explicit tasks. Levels of processing and task conditions differ only in the level of initial learning or availability. Thus, either the implicit and explicit task reflect traces in the same memory system or they reflect traces in different systems that have identical forgetting dynamics.

Odor memory: Review and analysis

We critically review the cognitive literature on olfactory memory and identify the similarities and differences between odor memory and visual-verbal memory. We then analyze this literature using criteria from a multiple memory systems approach to determine whether olfactory memory can be considered to be a separate memory system. We conclude that olfactory memory has a variety of important distinguishing characteristics, but that more data are needed to confer this distinction. We suggest methods for the study of olfactory memory that should make a resolution on the separate memory system hypothesis possible while simultaneously advancing a synthetic understanding of olfaction and cognition.

The role of decision processes in remembering and knowing

Participants in recognition memory studies are now often asked to partition recognized items into ones that are accompanied by some recollective experience (those they remember) and ones that are not so accompanied (but which they know were previously encountered). Rather than detecting separate memory systems, such attempts to distinguish between remembering and knowing are better understood as a division of positive recognition responses into those that lie above a second decision criterion (remember) and those that do not (know). As such, the amount of memory associated with knowing is strongly dependent on the placement of the decision criteria. A meta-analysis of published data and a simple experiment tested predictions from the decision process analysis of remember/know responses.

Who is mistaken about priming in “recognition/identification” experiments? A reply to tulving and hayman

Abstract Findings of stochastic independence between successive explicit and implicit memory measures are commonly interpreted as evidence that the two measures reflect the operation of separate memory systems. Ostergaard (1992) showed that often the contribution of memory to performance on one of the measures is small and that this may severely constrain the degree of dependence that the memory-related variance can produce in the overall contingency analysis of performance. Ostergaard (1992) developed the model of Maximum Memory Dependence (MMD) to estimate the consequences for the overall contingency analysis of maximum dependence between the components of the two measures that can be attributed to the prior study episode. The model was applied to a number of published studies and it was concluded that in most cases the memory-related variance could have produced only small and often insignificant effects on the overall contingency analysis. Tulving and Hayman (1993) claim that Ostergaard made a mistake...