Endel Tulving

Availability versus accessibility of information in memory for words.

The S s learned, on a single trial, lists of words belonging to explicitly designated conceptual categories. Lists varied in terms of length (12, 24, and 48 words) and number of words per category (1, 2, and 4). Immediate recall was tested either in presence or absence of category names as retrieval cues. Cued recall was higher than noncued recall, the difference varying directly with list length and inversely with number of items per category. This finding was interpreted as indicating that sufficiently intact memory traces of many words not recalled under the noncued recall conditions were available in the memory storage, but not accessible for retrieval. Further analysis of the data in terms of recall of categories and recall of words within recalled categories suggested two independent retrieval processes, one concerned with the accessibility of higher-order memory units, the other with accessibility of items within higher-order units.

Episodic and declarative memory: Role of the hippocampus

The fact that medial temporal lobe structures, including the hippocampus, are critical for declarative memory is firmly established by now. The understanding of the role that these structures play in declarative memory, however, despite great efforts spent in the quest, has eluded investigators so far. Given the existing scenario, novel ideas that hold the promise of clarifying matters should be eagerly sought. One such idea was recently proposed by Vargha‐Khadem and her colleagues (Science 1997;277:376–380) on the basis of their study of three young people suffering from anterograde amnesia caused by early‐onset hippocampal pathology. The idea is that the hippocampus is necessary for remembering ongoing lifes experiences (episodic memory), but not necessary for the acquisition of factual knowledge (semantic memory). We discuss the reasons why this novel proposal makes good sense and why it and its ramifications should be vigorously pursued. We review and compare declarative and episodic theories of amnesia, and argue that the findings reported by Vargha‐Khadem and her colleagues fit well into an episodic theory that retains components already publicized, and adds new ones suggested by the Vargha‐Khadem et al. study. Existing components of this theory include the idea that acquisition of factual knowledge can occur independently of episodic memory, and the idea that in anterograde amnesia it is quite possible for episodic memory to be more severely impaired than semantic memory. We suggest a realignment of organization of memory such that declarative memory is defined in terms of features and properties that are common to both episodic and semantic memory. The organization of memory thus modified gives greater precision to the Vargha‐Khadem et al. neuroanatomical model in which declarative memory depends on perihippocampal cortical regions but not on the hippocampus, whereas episodic memory, which is separate from declarative memory, depends on the hippocampus. Hippocampus 1998;8:198–204.

Précis of Elements of episodic memory

Elements of episodic memory (Tulving 1983b) consists of three parts. Part I argues for the distinction between episodic and semantic memory as functionally separate albeit closely interacting systems. It begins with a review of the 1972 essay on the topic (Tulving 1972) and its shortcomings, presents a somewhat more complete characterization of the two forms of memory than the one that was possible in 1972, and proceeds to discuss empirical and theoretical reasons for a tentative acceptance of the functional distinction between the two systems and its possible extensions. Part II describes a framework for the study of episodic memory, dubbed General Abstract Processing System (GAPS). The basic unit in such study is an act of remembering. It begins with the witnessing of an event and ends with recollective experience of the event, with related memory performance, or both. The framework specifies a number of components (elements) of the act of remembering and their interrelations, classified under two broad categories of encoding and retrieval. Part III discusses experimental research under the label of “synergistic ecphory.” Ecphory is one of the central elements of retrieval; “synergistic” refers to the joint influence that the stored episodic information and the cognitively present retrieval information exert on the construction of the product of ecphory, the so-called ecphoric information. The concept of encoding specificity and the phenomenon of recognition failure of recallable words figure prominently in Part III. The final chapter of the book describes a model, named the synergistic ecphory model of retrieval, that relates qualitative characteristics of recollective experience and quantitative measures of memory performance in recall and recognition to the conjunction of episodic-memory traces and semantic-memory retrieval cues.

PET studies of encoding and retrieval: The HERA model

We review positron emission tomography (PET) studies whose results converge on the hemispheric encoding/retrieval asymmetry (HERA) model of the involvement of prefrontal cortical regions in the processes of human memory. The model holds that the left prefrontal cortex is differentially more involved in retrieval of information from semantic memory, and in simultaneously encoding novel aspects of the retrieved information into episodic memory, than is the right prefrontal cortex. The right prefrontal cortex, on the other hand, is differentially more involved in episodic memory retrieval than is the left prefrontal cortex. This general pattern holds for different kinds of information (e.g., verbal materials, pictures, faces) and a variety of conditions of encoding and retrieval.

In Search of the Self: A Positron Emission Tomography Study

Previous work using positron emission tomography (PET) has shown that memory encoding processes are associated with preferential activation of left frontal regions of the brain, whereas retrieval processes are associated predominantly with right frontal activations. One possible reason for the asymmetry is that episodic retrieval necessarily involves reference to the self, and the self-concept may be represented (at least partially) in right frontal regions. Accordingly, the present study investigated the possibility that encoding of self-related material might also activate right frontal areas. Eight right-handed volunteers judged trait adjectives under four separate PET scan conditions: (a) relevance to self, (b) relevance to a well-known public figure, (c) social desirability, and (d) number of syllables. The results showed that self-related encoding yielded left frontal activations similar to those associated with other types of semantic encoding, but also specific activations in the right frontal lobe. It is concluded that the concept of self involves both general schematic structures and further specific components involved in episodic memory retrieval.

Hippocampal PET activations of memory encoding and retrieval: The HIPER model

A meta‐analysis of experimentally induced changes in blood flow (“activations”) in positron emission tomography (PET) studies of memory has revealed an orderly functional anatomic pattern: Activations in the hippocampal region associated with episodic memory encoding are located primarily in the rostral portions of the region, whereas activations associated with episodic memory retrieval are located primarily in the caudal portions. These findings are based on an analysis of a sample of 54 “hippocampal encoding and retrieval” activations that were culled from an overall database consisting of 52 published PET studies of memory. We refer to this general pattern of rostrocaudal gradient of encoding and retrieval PET activations as the HIPER (Hippocampal Encoding/Retrieval) model. The model suggests a division of memory‐related labor between the rostral and caudal portions of the hippocampal formation. Because functional anatomic pattern of encoding and retrieval activation that defines the HIPER model was unprecedented and unexpected, it is difficult to relate the model to what is already known or thought about functional neuroanatomy of episodic memory in the hippocampal regions. The model is interesting primarily because its exploration may yield fresh insights into the neural basis of human memory. Hippocampus 1998;8:313–322.

Hemispheric asymmetries of memory: the HERA model revisited

The hemispheric encoding/retrieval asymmetry (HERA) model is a process-specific description of experimental data provided by a large set of functional neuroimaging studies. According to HERA, left prefrontal cortex (PFC) is more involved than right PFC in episodic memory encoding, whereas right PFC is more involved than left PFC in episodic memory retrieval. Recently it has been claimed that this description does not hold for non-verbal materials. Here we propose a more precise formulation of HERA than previously, and argue that there is sufficient evidence to conclude that HERA, as reformulated, is true for both verbal and non-verbal materials.

Frontal lobe damage produces episodic memory impairment.

This article reports the outcome of a meta-analysis of the relation between the frontal lobes and memory as measured by tests of recognition, cued recall, and free recall. We reviewed experiments in which patients with documented, circumscribed frontal pathology were compared with normal control subjects on these three types of tests. Contrary to conventional wisdom, there is strong evidence that frontal damage disrupts performance on all three types of tests, with the greatest impairment in free recall, and the smallest in recognition.

Functional brain maps of retrieval mode and recovery of episodic information.

Positron emission tomography (PET) was used to identify brain regions associated with two component processes of episodic retrieval; those related to thinking back in subjective time (retrieval mode) and those related to actual recovery of stored information (ecphory). Healthy young subjects recognized words that had been encoded with respect to meaning or the speakers voice. Regardless of how the information had been encoded, recognition was associated with increased activation in regions in right prefrontal cortex, left anterior cingulate, and cerebellum. These activations reflect retrieval mode. Recognition following meaning encoding was specifically associated with increased activation in left temporal cortex, and recognition following voice encoding involved regions in right orbital frontal and parahippocampal cortex. These activations reflect ecphory of differentially encoded information.

Functional role of the prefrontal cortex in retrieval of memories: a PET study.

Retrieval of information from episodic memory involves the processes invoked by the attempt to remember (retrieval attempt) as well as processes associated with the successful retrieval of stored information (ecphory). Previous PET studies of memory have shown an activation of the prefrontal cortex in memory retrieval tasks, and we hypothesised that this activation represents retreival attempt, not ecphory. This hypothesis was directly directed using [15O]H2 PET imaging in 19 healthy subjects who performed three matched tasks which involved different levels of retrieval attempt and ecphory. The results showed that retrieval attempt was associated with activation of the prefrontal cortex, right greater than left, while ecphory involved the posterior cortical regions. These findings illuminate the functional role of the different neuroanatomical regions involved in episodic remembering.