Associative Retrieval Processes in Episodic Memory

Association and context constitute two of the central ideas in the history of episodic memory research. Following a brief discussion of the history of these ideas, we review data that demonstrate the complementary roles of temporal contiguity and semantic relatedness in determining the order in which subjects recall lists of items and the timing of their successive recalls. These analyses reveal that temporal contiguity effects persist over very long time scales, a result that challenges traditional psychological and neuroscientific models of association. The form of the temporal contiguity effect is conserved across all of the major recall tasks and even appears in item recognition when subjects respond with high confidence. The nearuniversal form of the contiguity effect and its appearance at diverse time scales is shown to place tight constraints on the major theories of association

Dynamics of brain activity reveal a unitary recognition signal.

Dual-process models of recognition memory typically assume that independent familiarity and recollec-tion signals with distinct temporal profiles can each lead to recognition (enabling 2 routes to recognition),whereas single-process models posit a unitary “memory strength” signal. Using multivariate classifierstrained on spectral electroencephalogram (EEG) features, we quantified neural evidence for recognitiondecisions as a function of time. Classifiers trained on a small portion of the decision period performedsimilarly to those also incorporating information from previous time points indicating that neural activityreflects an integrated evidence signal. We propose a single-route account of recognition memory that iscompatible with contributions from familiarity and recollection signals, but relies on a unitary evidencesignal that integrates all available evidence

Spatial Representations in the Human Brain

While extensive research on the neurophysiology of spatial memory has been carried out in rodents, memory research in humans had traditionally focused on more abstract, language-based tasks. Recent studies have begun to address this gap using virtual navigation tasks in combination with electrophysiological recordings in humans. These studies suggest that the human medial temporal lobe (MTL) is equipped with a population of place and grid cells similar to that previously observed in the rodent brain. Furthermore, theta oscillations have been linked to spatial navigation and, more specifically, to the encoding and retrieval of spatial information. While some studies suggest a single navigational theta rhythm which is of lower frequency in humans than rodents, other studies advocate for the existence of two functionally distinct delta–theta frequency bands involved in both spatial and episodic memory. Despite the general consensus between rodent and human electrophysiology, behavioral work in humans does not unequivocally support the use of a metric Euclidean map for navigation. Formal models of navigational behavior, which specifically consider the spatial scale of the environment and complementary learning mechanisms, may help to better understand different navigational strategies and their neurophysiological mechanisms. Finally, the functional overlap of spatial and declarative memory in the MTL calls for a unified theory of MTL function. Such a theory will critically rely upon linking task-related phenomena at multiple temporal and spatial scales. Understanding how single cell responses relate to ongoing theta oscillations during both the encoding and retrieval of spatial and non-spatial associations appears to be key toward developing a more mechanistic understanding of memory processes in the MTL

Auditory Short-Term Memory Behaves Like Visual Short-Term Memory

Are the information processing steps that support short-term sensory memory common to all the senses? Systematic, psychophysical comparison requires identical experimental paradigms and comparable stimuli, which can be challenging to obtain across modalities. Participants performed a recognition memory task with auditory and visual stimuli that were comparable in complexity and in their neural representations at early stages of cortical processing. The visual stimuli were static and moving Gaussian-windowed, oriented, sinusoidal gratings (Gabor patches); the auditory stimuli were broadband sounds whose frequency content varied sinusoidally over time (moving ripples). Parallel effects on recognition memory were seen for number of items to be remembered, retention interval, and serial position. Further, regardless of modality, predicting an item's recognizability requires taking account of (1) the probe's similarity to the remembered list items (summed similarity), and (2) the similarity between the items in memory (inter-item homogeneity). A model incorporating both these factors gives a good fit to recognition memory data for auditory as well as visual stimuli. In addition, we present the first demonstration of the orthogonality of summed similarity and inter-item homogeneity effects. These data imply that auditory and visual representations undergo very similar transformations while they are encoded and retrieved from memory

Synchronous and asynchronous theta and gamma activity during episodic memory formation.

To test the hypothesis that neural oscillations synchronize to mediate memory encoding, we analyzed electrocorticographic recordings taken as 68 human neurosurgical patients studied and subsequently recalled lists of common words. To the extent that changes in spectral power reflect synchronous oscillations, we would expect those power changes to be accompanied by increases in phase synchrony between the region of interest and neighboring brain areas. Contrary to the hypothesized role of synchronous gamma oscillations in memory formation, we found that many key regions that showed power increases during successful memory encoding also exhibited decreases in global synchrony. Similarly, cortical theta activity that decreases during memory encoding exhibits both increased and decreased global synchrony depending on region and stage of encoding. We suggest that network synchrony analyses, as used here, can help to distinguish between two major types of spectral modulations: (1) those that reflect synchronous engagement of regional neurons with neighboring brain areas, and (2) those that reflect either asynchronous modulations of neural activity or local synchrony accompanied by global disengagement from neighboring regions. We show that these two kinds of spectral modulations have distinct spatiotemporal profiles during memory encoding

Electrical Stimulation Modulates High γ Activity and Human Memory Performance.

Direct electrical stimulation of the brain has emerged as a powerful treatment for multiple neurological diseases, and as a potential technique to enhance human cognition. Despite its application in a range of brain disorders, it remains unclear how stimulation of discrete brain areas affects memory performance and the underlying electrophysiological activities. Here, we investigated the effect of direct electrical stimulation in four brain regions known to support declarative memory: hippocampus (HP), parahippocampal region (PH) neocortex, prefrontal cortex (PF), and lateral temporal cortex (TC). Intracranial EEG recordings with stimulation were collected from 22 patients during performance of verbal memory tasks. We found that high γ (62-118 Hz) activity induced by word presentation was modulated by electrical stimulation. This modulatory effect was greatest for trials with poor memory encoding. The high γ modulation correlated with the behavioral effect of stimulation in a given brain region: it was negative, i.e., the induced high γ activity was decreased, in the regions where stimulation decreased memory performance, and positive in the lateral TC where memory enhancement was observed. Our results suggest that the effect of electrical stimulation on high γ activity induced by word presentation may be a useful biomarker for mapping memory networks and guiding therapeutic brain stimulation

Theta and high-frequency activity mark spontaneous recall of episodic memories.

Humans possess the remarkable ability to search their memory, allowing specific past episodes to be re-experienced spontaneously. Here, we administered a free recall test to 114 neurosurgical patients and used intracranial theta and high-frequency activity (HFA) to identify the spatiotemporal pattern of neural activity underlying spontaneous episodic retrieval. We found that retrieval evolved in three electrophysiological stages composed of: (1) early theta oscillations in the right temporal cortex, (2) increased HFA in the left hemisphere including the medial temporal lobe (MTL), left inferior frontal gyrus, as well as the ventrolateral temporal cortex, and (3) motor/language activation during vocalization of the retrieved item. Of these responses, increased HFA in the left MTL predicted recall performance. These results suggest that spontaneous recall of verbal episodic memories involves a spatiotemporal pattern of spectral changes across the brain; however, high-frequency activity in the left MTL represents a final common pathway of episodic retrieval

Recall termination in free recall

Although much is known about the dynamics of memory search in the free recall task, relatively little is known about the factors related to recall termination. Reanalyzing individual trial data from 14 prior studies (1,079 participants in 28,015 trials) and defining termination as occurring when a final response is followed by a long nonresponse interval, we observed that termination probability increased throughout the recall period and that retrieval was more likely to terminate following an error than following a correct response. Among errors, termination probability was higher following prior-list intrusions and repetitions than following extralist intrusions. To verify that this pattern of results can be seen in a single study, we report a new experiment in which 80 participants contributed recall data from a total of 9,122 trials. This experiment replicated the pattern observed in the aggregate analysis of the prior studies