Ken A. Paller

Observing the transformation of experience into memory

The ability to remember ones past depends on neural processing set in motion at the moment each event is experienced. Memory formation can be observed by segregating neural responses according to whether or not each event is recalled or recognized on a subsequent memory test. Subsequent memory analyses have been performed with various neural measures, including brain potentials extracted from intracranial and extracranial electroencephalographic recordings, and hemodynamic responses from functional magnetic resonance imaging. Neural responses can predict which events, and which aspects of those events, will be subsequently remembered or forgotten, thereby elucidating the neurocognitive processes that establish durable episodic memories.

Brain potentials during memory retrieval provide neurophysiological support for the distinction between conscious recollection and priming

Event-related brain potentials were recorded from subjects as they attempted to identify words displayed tachistoscopically. Words that had also been presented a few minutes earlier in a different context were identified more often than were words that had not been presented before. This priming effect was observed for words initially seen in an imagery task requiring size estimations as well as for words initially seen in an orthographic task requiring letter counting. Unlike priming, recall and recognition were much better for words repeated from the imagery task than from the orthographic task. Brain potentials elicited during word identification also differed as a function of task. Based on these differences, a potential from 500 to 800 msec was interpreted as an index of recollection processes. Earlier potentials may have indexed processing related to priming. These effects thus provide measures of the hypothetical processes underlying memory performance and demonstrate that recollection and priming are associated with distinct neural events.

Validating neural correlates of familiarity

Familiarity is a pervasive memory phenomenon that occurs in its most basic form when someone recognizes a repeated stimulus without recollecting other aspects of the requisite prior learning episode. Theoretical controversy currently abounds with respect to both the cognitive and neural characteristics of familiarity. Here, we show that the extant data, particularly brain-potential data, are insufficient for validating putative neural correlates of familiarity, and we outline strategies for making progress on this problem. Conceptual priming is an implicit-memory phenomenon that often occurs together with familiarity; experiments that conflate the two phenomena can be misleading. Avoiding this conflation is required to understand familiarity and to determine the extent to which the neurocognitive processes that support priming also drive familiarity.

Strengthening Individual Memories by Reactivating Them During Sleep

During sleep, memories can be influenced in a specific and systematic manner. While asleep, people heard sounds that had earlier been associated with objects at specific spatial locations. Upon waking, they recalled these locations more accurately than other locations for which no reminder cues were provided. Consolidation thus operates during sleep with high specificity and is subject to systematic influences through simple auditory stimulation.

Monitoring Conscious Recollection via the Electrical Activity of the Brain

Although another persons experience of recollection cannot be observed directly, we have found that the underlying operations can be monitored using noninvasive electrophysiological techniques Results from two experiments showed that brain potentials elicited 500 to 900 ms after the onset of visually presented words vary systematically in amplitude with manipulations that influence the extent to which subjects engage in recollective processing These brain potentials can thus be construed as correlates of the subjective experience of recollection

Recall and Stem-Completion Priming Have Different Electrophysiological Correlates and Are Modified Differentially by Directed Forgetting

The notion that different aspects of memory are assessed by explicit and implicit memory tests was supported by behavioral and electrophysiological results. In a study-test procedure, 24 subjects were instructed to remember some words and to forget other words. Free recall and cued recall were better for words associated with the remember instruction, whereas directed forgetting did not influence stem completion (an implicit memory test). Event-related brain potentials elicited during study differed as a function of subsequent memory performance for free recall and cued recall, but not for stem completion. These results implicate encoding differences in the distinction between the 2 types of memory test. Factors governing whether explicit retrieval affects performance on an implicit memory test, mechanisms that may underlie directed-forgetting effects, and the importance of electrophysiological correlates of memory are also discussed.

Brain networks for analyzing eye gaze.

The eyes convey a wealth of information in social interactions. This information is analyzed by multiple brain networks, which we identified using functional magnetic resonance imaging (MRI). Subjects attempted to detect a particular directional cue provided either by gaze changes on an image of a face or by an arrow presented alone or by an arrow superimposed on the face. Another control condition was included in which the eyes moved without providing meaningful directional information. Activation of the superior temporal sulcus accompanied extracting directional information from gaze relative to directional information from an arrow and relative to eye motion without relevant directional information. Such selectivity for gaze processing was not observed in face-responsive fusiform regions. Brain activations were also investigated while subjects viewed the same face but attempted to detect when the eyes gazed directly at them. Most notably, amygdala activation was greater during periods when direct gaze never occurred than during periods when direct gaze occurred on 40% of the trials. In summary, our results suggest that increases in neural processing in the amygdala facilitate the analysis of gaze cues when a person is actively monitoring for emotional gaze events, whereas increases in neural processing in the superior temporal sulcus support the analysis of gaze cues that provide socially meaningful spatial information.

Neural correlates of memory retrieval and evaluation

Results from recent neuroimaging studies have led to a controversy as to whether right or left prefrontal regions are relatively more important for episodic retrieval. To address this issue, we recorded event-related brain potentials during two recognition tests with identical stimuli but differing retrieval demands. In both tests, participants viewed a sequence of object drawings, half of which were identical to ones viewed earlier except for a change in size and half of which were new. Instructions were to discriminate between old and new objects (general test) or to additionally decide whether old objects were larger or smaller at study (specific test). Frontal brain potentials that were more positive during the specific than during the general test for both old and new objects were interpreted as neural correlates of the process by which specific attributes of test cues are compared with information retrieved from memory. Another ERP difference between the specific and general tests, which was observed for old objects only, had a left posterior scalp topography and was interpreted to reflect the reactivation of memories for studied objects. Frontal and posterior potentials thus reflected two memory processes important for accurate episodic retrieval. Furthermore, our findings suggest that both left and right prefrontal regions were engaged when demands to retrieve and evaluate perceptual information increased.

When memory does not fail: familiarity-based recognition in mild cognitive impairment and Alzheimer's disease.

Recognition can be guided by familiarity, a restricted form of retrieval devoid of contextual recall, or by recollection, which occurs when retrieval is sufficient to support the full experience of remembering an episode. Recollection and familiarity were disentangled by testing recognition memory using silhouette object drawings, high target-foil resemblance, and both yes-no and forced-choice procedures. Theoretically, forced-choice recognition could be mediated by familiarity alone. Alzheimers disease and its preclinical stage, mild cognitive impairment (MCI), were associated with memory impairments that were greater on the yes-no test. Remarkably, forced-choice recognition was unequivocally normal in patients with MCI compared with age-matched controls. Neuropathology in hippocampus and entorhinal cortex, known to be present in MCI, presumably disrupted recollection while leaving familiarity-based recognition intact.

Attention induces synchronization-based response gain in steady-state visual evoked potentials.

When attention is voluntarily directed to a spatial location, visual sensitivity increases at that location. What causes this improved sensitivity? Studies of single neuron spike rates in monkeys have provided mixed results in regard to whether attending to a stimulus increases its effective contrast (contrast gain) or multiplicatively boosts stimulus-driven neural responses (response or activity gain). We monitored frequency-tagged steady-state visual evoked potentials (SSVEPs) in humans and found that voluntary sustained attention multiplicatively increased stimulus-driven population electrophysiological activity. Analyses of intertrial phase coherence showed that this attentional response gain was at least partially due to the increased synchronization of SSVEPs to stimulus flicker. These results suggest that attention operates in a complementary manner at different levels; attention seems to increase single-neuron spike rates in a variety of ways, including contrast, response and activity gains, while also inducing a multiplicative boost on neural population activity via enhanced response synchronization.