Spontaneous revisitation during visual exploration as a link among strategic behavior, learning, and the hippocampus.

Effective exploratory behaviors involve continuous updating of sensory sampling to optimize the efficacy of information gathering. Despite some work on this issue in animals, little information exists regarding the cognitive or neural mechanisms for this sort of behavioral optimization in humans. Here we examined a visual exploration phenomenon that occurred when human subjects studying an array of objects spontaneously looked "backward" in their scanning paths to view recently seen objects again. This "spontaneous revisitation" of recently viewed objects was associated with enhanced hippocampal activity and superior subsequent memory performance in healthy participants, but occurred only rarely in amnesic patients with severe damage to the hippocampus. These findings demonstrate the necessity of the hippocampus not just in the aspects of long-term memory with which it has been associated previously, but also in the short-term adaptive control of behavior. Functional neuroimaging showed hippocampal engagement occurring in conjunction with frontocerebellar circuits, thereby revealing some of the larger brain circuitry essential for the strategic deployment of information-seeking behaviors that optimize learning.

Stuck in the past: neural events that predict intrusions from prior trials.

Neurologically intact adults perseverate in immediate serial recall, intruding items from a previous trial into the current response. We applied the electroencephalogram/event-related-potential subsequent-memory paradigm to immediate serial recall to investigate the causes of these errors. In line with previous studies using this paradigm, results revealed that words that were correctly recalled elicited a greater frontal positivity during encoding when compared with words that were either perseverated over or not produced for some other reason. More surprisingly, differences were also found at encoding between the words perseverated into the subsequent response and words that were not perseverated. These findings support a theory stating that abnormalities in both how the current target and the previous trial are processed can contribute to perseveration errors. These results inform existing theories of immediate serial recall and theories of the control of irrelevant information.

Comparison of neural activity that leads to true memories, false memories, and forgetting: An fMRI study of the misinformation effect.

False memories can occur when people are exposed to misinformation about a past event. Of interest here are the neural mechanisms of this type of memory failure. In the present study, participants viewed photographic vignettes of common activities during an original event phase (OEP), while we monitored their brain activity using fMRI. Later, in a misinformation phase, participants viewed sentences describing the studied photographs, some of which contained information conflicting with that depicted in the photographs. One day later, participants returned for a surprise item memory recognition test for the content of the photographs. Results showed reliable creation of false memories, in that participants reported information that had been presented in the verbal misinformation but not in the photographs. Several regions were more active during the OEP for later accurate memory than for forgetting, but they were also more active for later false memories, indicating that false memories in this paradigm are not simply caused by failure to encode the original event. There was greater activation in the ventral visual stream for subsequent true memories than for subsequent false memories, however, suggesting that differences in encoding may contribute to later susceptibility to misinformation.

Memory strength and repetition suppression: multimodal imaging of medial temporal cortical contributions to recognition.

Declarative memory permits an organism to recognize stimuli that have been previously encountered, discriminating them from those that are novel. One basis for recognition is item memory strength, which may support the perception of stimulus familiarity. Though the medial temporal lobes are known to be critical for declarative memory, at present the neural mechanisms supporting perceived differences in memory strength remain poorly specified. Here, functional MRI (fMRI) and anatomically constrained magnetoencephalography (MEG) indexed correlates of graded memory strength in the human brain, focusing on medial temporal cortex. fMRI revealed a decrease in medial temporal cortical activation that tracked parametric levels of perceived memory strength. Anatomically constrained MEG current estimates revealed that strength-dependent signal reductions onset within 150-300 ms. Memory strength appears to be rapidly signaled by medial temporal cortex through repetition suppression (activation reductions), providing a basis for the subjective perception of stimulus familiarity or novelty.

Activation of stimulus-specific processing regions at retrieval tracks the strength of relational memory.

Many theories of episodic memory posit that the subjective experience of recollection may be driven by the activation of stimulus-specific cortical regions during memory retrieval. This study examined cortical activation during associative memory retrieval to identify brain regions that support confidence judgments of source memory in stimulus-specific ways. Adjectives were encoded with either a picture of a face or a scene. During a source memory test, the word was presented alone and the participant was asked if the word had been previously paired with a face or a scene. We identified brain regions that were selectively active when viewing pictures of scenes or faces with a separate localizer scan. We then identified brain regions that were differentially activated to words during the source memory test that had been previously paired with faces or scenes, masked by the localizer activations, and examined how those regions were modulated by the strength of the source memory. Bilateral amygdala activation tracked source memory confidence for faces, while parahippocampal cortex tracked source memory confidence for scenes. The magnitude of the activation of these domain-specific perceptual-processing brain regions during memory retrieval may contribute to the subjective strength of episodic recollection.

Neural processing of recollection, familiarity and priming at encoding: evidence from a forced-choice recognition paradigm.

The distinction between neural mechanisms of explicit and implicit expressions of memory has been well studied at the retrieval stage, but less at encoding. In addition, dissociations obtained in many studies are complicated by methodological difficulties in obtaining process-pure measures of different types of memory. In this experiment, we applied a subsequent memory paradigm and a two-stage forced-choice recognition test to classify study ERP data into four categories: subsequent remembered (later retrieved accompanied by detailed information), subsequent known (later retrieved accompanied by a feeling of familiarity), subsequent primed (later retrieved without conscious awareness) and subsequent forgotten (not retrieved). Differences in subsequent memory effects (DM effects) were measured by comparing ERP waveform associated with later memory based on recollection, familiarity or priming with ERP waveform for later forgotten items. The recollection DM effect involved a robust sustained (onset at 300 ms) prefrontal positive-going DM effect which was right-lateralized, and a later (onset at 800 ms) occipital negative-going DM effect. Familiarity involved an earlier (300-400 ms) prefrontal positive-going DM effect and a later (500-600 ms) parietal positive-going DM effect. Priming involved a negative-going DM effect which onset at 600 ms, mainly distributed over anterior brain sites. These results revealed a sequence of components that represented cognitive processes underlying the encoding of verbal information into episodic memory, and separately supported later remembering, knowing and priming.

Event-related potential evidence suggesting voters remember political events that never happened.

Voters tend to misattribute issue positions to political candidates that are consistent with their partisan affiliation, even though these candidates have never explicitly stated or endorsed such stances. The prevailing explanation in political science is that voters misattribute candidates' issue positions because they use their political knowledge to make educated but incorrect guesses. We suggest that voter errors can also stem from a different source: false memories. The current study examined event-related potential (ERP) responses to misattributed and accurately remembered candidate issue information. We report here that ERP responses to misattributed information can elicit memory signals similar to that of correctly remembered old information--a pattern consistent with a false memory rather than educated guessing interpretation of these misattributions. These results suggest that some types of voter misinformation about candidates may be harder to correct than previously thought.

Using fMR-adaptation to track complex object representations in perirhinal cortex.

Brain regions in medial temporal lobe have seen a shift in emphasis in their role in long-term declarative memory to an appreciation of their role in cognitive domains beyond declarative memory, such as implicit memory, working memory, and perception. Recent theoretical accounts emphasize the function of perirhinal cortex in terms of its role in the ventral visual stream. Here, we used functional magnetic resonance adaptation (fMRa) to show that brain structures in the visual processing stream can bind item features prior to the involvement of hippocampal binding mechanisms. Evidence for perceptual binding was assessed by comparing BOLD (blood-oxygen-level-dependent) responses between fused objects and variants of the same object as different, non-fused forms (e.g., physically separate objects). Adaptation of the neural response to fused, but not non-fused, objects was in left fusiform cortex and left perirhinal cortex, indicating the involvement of these regions in the perceptual binding of item representations.

An ERP investigation into the strategic regulation of the fluency heuristic during recognition memory.

The goal of the present study was to determine whether masked repetition priming affects ERPs differently depending on whether or not participants are biased by task conditions to interpret enhanced perceptual fluency as evidence of prior study. Participants studied a list of words either in the visual modality or in the auditory modality and then performed a visual recognition memory test while ERPs were recorded. During the test, half the stimuli were preceded by a briefly presented matching prime word and half were preceded by a briefly presented non-matching prime word. Unlike in previous behavioral studies, masked repetition priming led to a reduction in positive recognition responses following auditory study, and had no effect following visual study, although post hoc analyses suggest that participants who received the visual study list may have relied on fluency to make some of their recognition decisions. Masked repetition priming also led to positive ERPs during two time windows-an early 300-500 ms window and a later 500-700 ms window. During the later time window, masked repetition priming exhibited a frontal scalp distribution that was most pronounced for participants who received the auditory study list. We suggest that this late frontal effect reflects participants' tendency to reject enhanced perceptual fluency as evidence of prior study.

Remembering and Voting: Theory and Evidence from Amnesic Patients.

One of the most prominent claims to emerge from the field of public opinion is that citizens can vote for candidates whose issue positions best reflect their own beliefs even when they cannot remember previously learned stances associated with the candidates. The current experiment provides a unique and powerful examination of this claim by determining whether individuals with profound amnesia, whose severe memory impairments prevent them from remembering specific issue information associated with any particular candidate, can vote for candidates whose issue positions come closest to their own political views. We report here that amnesic patients, despite not being able to remember any issue information, consistently voted for candidates with favored political positions. Thus, sound voting decisions do not require recall or recognition of previously learned associations between candidates and their issue positions. This result supports a multiple memory systems model of political decision making.

Cortical regions recruited for complex active-learning strategies and action planning exhibit rapid reactivation during memory retrieval.

Memory retrieval can involve activity in the same sensory cortical regions involved in perception of the original event, and this neural "reactivation" has been suggested as an important mechanism of memory retrieval. However, it is still unclear if fragments of experience other than sensory information are retained and later reactivated during retrieval. For example, learning in non-laboratory settings generally involves active exploration of memoranda, thus requiring the generation of action plans for behavior and the use of strategies deployed to improve subsequent memory performance. Is information pertaining to action planning and strategic processing retained and reactivated during retrieval? To address this question, we compared ERP correlates of memory retrieval for objects that had been studied in an active manner involving action planning and strategic processing to those for objects that had been studied passively. Memory performance was superior for actively studied objects, and unique ERP retrieval correlates for these objects were identified when subjects remembered the specific spatial locations at which objects were studied. Early-onset frontal shifts in ERP correlates of retrieval were noted for these objects, which parallel the recruitment of frontal cortex during learning object locations previously identified using fMRI with the same paradigm. Notably, ERPs during recall for items studied with a specific viewing strategy localized to the same supplementary motor cortex region previously identified with fMRI when this strategy was implemented during study, suggesting rapid reactivation of regions directly involved in strategic action planning. Collectively, these results implicate neural populations involved in learning in important retrieval functions, even for those populations involved in strategic control and action planning. Notably, these episodic features are not generally reported during recollective experiences, suggesting that reactivation is a more general property of memory retrieval that extends beyond those fragments of perceptual information that might be needed to re-live the past.

Hippocampal brain-network coordination during volitional exploratory behavior enhances learning.

Exploratory behaviors during learning determine what is studied and when, helping to optimize subsequent memory performance. To elucidate the cognitive and neural determinants of exploratory behaviors, we manipulated the control that human subjects had over the position of a moving window through which they studied objects and their locations. Our behavioral, neuropsychological and neuroimaging data indicate that volitional control benefits memory performance and is linked to a brain network that is centered on the hippocampus. Increases in correlated activity between the hippocampus and other areas were associated with specific aspects of memory, which suggests that volitional control optimizes interactions among specialized neural systems through the hippocampus. Memory is therefore an active process that is intrinsically linked to behavior. Furthermore, brain structures that are typically seen as passive participants in memory encoding (for example, the hippocampus) are actually part of an active network that controls behavior dynamically as it unfolds.

Event-related potential correlates of item and source memory strength.

Event-related potential (ERP) studies of recognition memory have shown dissociations between item recognition and source memory, wherein item recognition is associated with the mid-frontal FN400 component, which varies continuously with item memory strength, while source memory is associated with the late parietal effect (LPC). There is current debate about whether source memory can vary along a continuum of memory strength or is a threshold process. The LPC has been shown to be generally sensitive to correct versus incorrect source judgments, but varying levels of "source strength" along a single dimension of source evidence have not been tested. The current experiment had participants encode novel visual objects in one of two different task contexts by performing either a conceptual or perceptual judgment about the object. On a subsequent memory test, participants made an old/new decision on a 4-point confidence scale followed by a source memory confidence judgment, in which they indicated their confidence about which task they had performed with the object at encoding. ERPs from the memory test were examined for electrophysiological correlates of both item and source memory strength. Item memory was associated with differences in the 300-500 ms time window, consistent with the timing of the FN400. Differences in the amplitude of the LPC were observed between correct and incorrect source decisions, consistent with previous findings. Comparing low and high confidence source decisions also revealed differences, suggesting that the LPC is also sensitive to variations in the strength of source memory.

Time to go our separate ways: opposite effects of study duration on priming and recognition reveal distinct neural substrates.

Amnesic patients have difficulties recognizing when stimuli are repeated, even though their responses to stimuli can change as a function of repetition in indirect tests of memory - a pattern known as priming without recognition. Likewise, experimental manipulations can impair recognition in healthy individuals while leaving priming relatively unaffected, and priming and recognition have been associated with distinct neural correlates in these circumstances. Does this evidence necessarily indicate that priming and recognition rely on distinct brain systems? An alternative explanation is that recognition is merely more sensitive to amnestic insults and experimental manipulations than is priming, and that both priming and recognition are produced by a single brain system. If so, then experimental manipulations would tend to drive priming and recognition in the same direction, albeit to a greater extent for one versus the other in some circumstances. We found evidence to the contrary - that manipulating study duration has opposite effects on priming versus recognition. Studying objects for one-quarter second led to worse recognition than studying objects for 2 s, whereas the opposite was true for priming (greater for one-quarter-second study than two-second study). Furthermore, distinct electrophysiological repetition effects were associated with priming versus recognition. We therefore conclude that study duration had opposite effects on priming and recognition, and on the engagement of implicit versus explicit memory systems. These findings call into question single-process accounts of priming and recognition, and substantiate previous behavioral, neuropsychological, and neuroimaging dissociations between implicit and explicit memory.

Brain Imaging, Cognitive Processes, and Brain Networks.

The recent, rapid expansion of the application of neuroimaging techniques to a broad variety of questions about the structure and function of mind and brain has led to much necessary and often critical introspection about what these techniques can actually tell us about cognitive processes. In this article, we attempt to place neuroimaging within the broader context of the cognitive neuroscience approach, which emphasizes the benefits of converging methodologies for understanding cognition and how it is supported by the functioning of the brain. Our arguments for what neuroimaging has to offer are supported by two specific examples from research on memory that, we believe, show how neuroimaging data have provided unique insights not only into brain organization, but also into the organization of the mind.