Daniel S. Rizzuto

Reset of human neocortical oscillations during a working memory task

Both amplitude and phase of rhythmic slow-wave electroencephalographic activity are physiological correlates of learning and memory in rodents. In humans, oscillatory amplitude has been shown to correlate with memory; however, the role of oscillatory phase in human memory is unknown. We recorded intracranial electroencephalogram from human cortical and hippocampal areas while subjects performed a short-term recognition memory task. On each trial, a series of four list items was presented followed by a memory probe. We found agreement across trials of the phase of oscillations in the 7- to 16-Hz range after randomly timed stimulus events, evidence that these events either caused a phase shift in the underlying oscillation or initiated a new oscillation. Phase locking in this frequency range was not generally associated with increased poststimulus power, suggesting that stimulus events reset the phase of ongoing oscillations. Different stimulus classes selectively modulated this phase reset effect, with topographically distinct sets of recording sites exhibiting preferential reset to either probe items or to list items. These findings implicate the reset of brain oscillations in human working memory.

Human neocortical oscillations exhibit theta phase differences between encoding and retrieval.

We analyzed intracranial brain activity recorded from human participants during the performance of a working-memory task. We show that 6-13 Hz activity exhibits consistent phase across trials following experimental stimuli, and that this phase significantly differs between study and test stimuli. These findings suggest that oscillatory phase reflects the encoding-retrieval state of neural networks, supporting predictions of recent models of memory.[Hasselmo, M.E., Wyble, B.P., and Bodelon, C., 2002. A proposed function for hippocampal theta rhythm: Separate phases of encoding and retrieval enhance reversal of prior learning. Neural Comput. 14 793-817.; Judge, S.J., Hasselmo, M.E., 2004. Theta rhythmic stimulation of stratum lacunosum-moleculare in rat hippocampus contributes to associative LTP at a phase offset in stratum radiatum. J. Neurophys. 92 1516-1624.].

An Autoassociative Neural Network Model of Paired-Associate Learning

Hebbian heteroassociative learning is inherently asymmetric. Storing a forward association, from item A to item B, enables recall of B (given A), but does not permit recall of A (given B). Recurrent networks can solve this problem by associating A to B and B back to A. In these recurrent networks, the forward and backward associations can be differentially weighted to account for asymmetries in recall performance. In the special case of equal strength forward and backward weights, these recurrent networks can be modeled as a single autoassociative network where A and B are two parts of a single, stored pattern. We analyze a general, recurrent neural network model of associative memory and examine its ability to fit a rich set of experimental data on human associative learning. The model fits the data significantly better when the forward and backward storage strengths are highly correlated than when they are less correlated. This network-based analysis of associative learning supports the view that associations between symbolic elements are better conceptualized as a blending of two ideas into a single unit than as separately modifiable forward and backward associations linking representations in memory.

Spatial selectivity in human ventrolateral prefrontal cortex

The functional organization of lateral prefrontal cortex is not well understood, and there is debate as to whether the dorsal and ventral aspects mediate distinct spatial and non-spatial functions, respectively. We show for the first time that recordings from human ventrolateral prefrontal cortex show spatial selectivity, supporting the idea that ventrolateral prefrontal cortex is involved in spatial processing. Our results also indicate that prefrontal cortex may be a source of control signals for neuroprosthetic applications.

Theoretical correlations and measured correlations: relating recognition and recall in four distributed memory models.

This article addresses the relation between item recognition and associative (cued) recall. Going beyond measures of performance on each task, the analysis focuses on the degree to which the contingency between successful recognition and successful recall of a studied item reflects the commonality of memory processes underlying the recognition and recall tasks. Specifically, 4 classes of distributed memory models are assessed for their ability to account for the relatively invariant correlation (approximately .5) between successive recognition and recall. Basic versions of each model either under- or overpredict the intertask correlation. Introducing variability in goodness-of-encoding and response criteria, as well as output encoding, enabled all 4 models to reproduce the moderate intertask correlation and the increase in correlation observed in 2 mixed-list experiments. This model-based analysis provides a general theoretical framework for interpreting contingencies between successive memory tests.

Direct Brain Stimulation Modulates Encoding States and Memory Performance in Humans

People often forget information because they fail to effectively encode it. Here, we test the hypothesis that targeted electrical stimulation can modulate neural encoding states and subsequent memory outcomes. Using recordings from neurosurgical epilepsy patients with intracranially implanted electrodes, we trained multivariate classifiers to discriminate spectral activity during learning that predicted remembering from forgetting, then decoded neural activity in later sessions in which we applied stimulation during learning. Stimulation increased encoding-state estimates and recall if delivered when the classifier indicated low encoding efficiency but had the reverse effect if stimulation was delivered when the classifier indicated high encoding efficiency. Higher encoding-state estimates from stimulation were associated with greater evidence of neural activity linked to contextual memory encoding. In identifying the conditions under which stimulation modulates memory, the data suggest strategies for therapeutically treating memory dysfunction.

Temporal associative processes revealed by intrusions in paired-associate recall

Although much is known about the factors that influence the acquisition and retention of individual paired associates, the existence of temporally defined associations spanning multiple pairs has not been demonstrated. We report two experiments in which subjects studied randomly paired nouns for a subsequent cued recall test. When subjects recalled nontarget items, their intrusions tended to come from nearby pairs. This across-pair contiguity effect was graded, spanning noncontiguously studied word pairs. The existence of such long-range temporally defined associations lends further support to contextual-retrieval models of episodic association.

Associative symmetry vs. independent associations

Abstract We develop a neural network model of paired-associate learning based upon an auto-associative learning mechanism. We show that this relatively simple neural network can replicate complex human behavioral data, but only when the correlation between forward and backward learning is highly correlated. This network-based analysis is used to constrain psychological theories of association in humans.

Closed-loop stimulation of temporal cortex rescues functional networks and improves memory

Memory failures are frustrating and often the result of ineffective encoding. One approach to improving memory outcomes is through direct modulation of brain activity with electrical stimulation. Previous efforts, however, have reported inconsistent effects when using open-loop stimulation and often target the hippocampus and medial temporal lobes. Here we use a closed-loop system to monitor and decode neural activity from direct brain recordings in humans. We apply targeted stimulation to lateral temporal cortex and report that this stimulation rescues periods of poor memory encoding. This system also improves later recall, revealing that the lateral temporal cortex is a reliable target for memory enhancement. Taken together, our results suggest that such systems may provide a therapeutic approach for treating memory dysfunction.Memory lapses can occur due to ineffective encoding, but it is unclear if targeted brain stimulation can improve memory performance. Here, authors use a closed-loop system to decode and stimulate periods of ineffective encoding, showing that stimulation of lateral temporal cortex can enhance memory.

Widespread theta synchrony and high-frequency desynchronization underlies enhanced cognition

The idea that synchronous neural activity underlies cognition has driven an extensive body of research in human and animal neuroscience. Yet, insufficient data on intracranial electrical connectivity has precluded a direct test of this hypothesis in a whole-brain setting. Through the lens of memory encoding and retrieval processes, we construct whole-brain connectivity maps of fast gamma (30–100 Hz) and slow theta (3–8 Hz) spectral neural activity, based on data from 294 neurosurgical patients fitted with indwelling electrodes. Here we report that gamma networks desynchronize and theta networks synchronize during encoding and retrieval. Furthermore, for nearly all brain regions we studied, gamma power rises as that region desynchronizes with gamma activity elsewhere in the brain, establishing gamma as a largely asynchronous phenomenon. The abundant phenomenon of theta synchrony is positively correlated with a brain region’s gamma power, suggesting a predominant low-frequency mechanism for inter-regional communication.Synchronous neural activity is related with memory encoding and retrieval, but it is not clear whether this happens across the whole brain. Here, authors use intracranial recordings to show that gamma networks are largely asynchronous, desynchronizing while theta synchronizes during memory encoding and retrieval.