Distinct Neural Suppression and Encoding Effects for Conceptual Novelty and Familiarity.

Like yin and yang, novelty and familiarity are typically described as separate-yet-complementary aspects of an experience, two ends of a single continuum. However, novelty and familiarity are also multifaceted. For instance, novelty can sometimes result in enhanced mnemonic performance, whereas at other times familiarity is better remembered. As previous investigations focused primarily on the experimental aspect of novelty, the mechanisms supporting conceptual novelty (the novel combination of two previously unrelated existing concepts) remain unclear. Importantly, conceptual novelty can be recognized as such only when compared with preexperimental familiar knowledge, regardless of experimental status. Here we applied a combined repetition suppression/subsequent memory fMRI paradigm, focusing on the conceptual aspect of novelty and familiarity as the subject matter. Conceptual novelty was characterized by sustained neural activity; familiarity, on the other hand, exhibited repetition effects in multiple cortical regions, a subset of which was modulated by successful encoding. Subsequent memory of novelty was associated only with activation differences in a distinct set of regions, including the hippocampus and medial cortical regions. These results suggest that conceptual novelty (a) does not (easily) trigger the repetition suppression phenomenon but requires sustained neural recruitment and (b) activates dedicated encoding mechanisms. Conceptual familiarity, in contrast, allows rapid neural processing that depends upon existing neural representations. Overall, these findings challenge the definition of novelty as a unitary concept. Furthermore, they bear important implications for research into the neural bases of knowledge representation and recognition memory.

The effects of an action's "age-of-acquisition" on action-sentence processing.

How does our brain allow us comprehend abstract/symbolic descriptions of human action? Whereas past research suggested that processing action language relies on sensorimotor brain regions, recent work suggests that sensorimotor activation depends on participants' task goals, such that focusing on abstract (vs. concrete) aspects of an action activates "default mode network" (rather than sensorimotor) regions. Following a Piagetian framework, we hypothesized that for actions acquired at an age wherein abstract/symbolic cognition is fully-developed, even when participants focus on the concrete aspects of an action, they should retrieve abstract-symbolic mental representations. In two studies, participants processed the concrete (i.e., "how") and abstract (i.e., "why") aspects of late-acquired and early-acquired actions. Consistent with previous research, focusing on the abstract (vs. concrete) aspects of an action resulted in greater activation in the "default mode network". Importantly, the activation in these regions was higher when processing later-acquired (vs. earlier acquired) actions-also when participants' goal was to focus on the concrete aspects of the action. We discuss the implications of the current findings to research on the involvement of concrete representations in abstract cognition.

Reading and doing arithmetic nonconsciously.

The modal view in the cognitive and neural sciences holds that consciousness is necessary for abstract, symbolic, and rule-following computations. Hence, semantic processing of multiple-word expressions, and performing of abstract mathematical computations, are widely believed to require consciousness. We report a series of experiments in which we show that multiple-word verbal expressions can be processed outside conscious awareness and that multistep, effortful arithmetic equations can be solved unconsciously. All experiments used Continuous Flash Suppression to render stimuli invisible for relatively long durations (up to 2,000 ms). Where appropriate, unawareness was verified using both objective and subjective measures. The results show that novel word combinations, in the form of expressions that contain semantic violations, become conscious before expressions that do not contain semantic violations, that the more negative a verbal expression is, the more quickly it becomes conscious, and that subliminal arithmetic equations prime their results. These findings call for a significant update of our view of conscious and unconscious processes.

The language of future-thought: an fMRI study of embodiment and tense processing.

The ability to comprehend and represent the temporal properties of an occurrence is a crucial aspect of human language and cognition. Despite advances in neurolinguistic research into semantic processing, surprisingly little is known regarding the mechanisms which support the comprehension of temporal semantics. We used fMRI to investigate neural activity associated with processing of concrete and abstract sentences across the three temporal categories: past, present, and future. Theories of embodied cognition predict that concreteness-related activity would be evident in sensory and motor areas regardless of tense. Contrastingly, relying upon construal level theory we hypothesized that: (1) the neural markers associated with concrete language processing would appear for past and present tense sentences, but not for future sentences; (2) future tense sentences would activate intention-processing areas. Consistent with our first prediction, the results showed that activation in the parahippocampal gyrus differentiated between concrete and abstract sentences for past and present tense sentences, but not for future sentences. Not consistent with our second prediction, future tense sentences did not activate most of the regions that are implicated in the processing of intentions, but only activated the vmPFC. We discuss the implications of the current results to theories of embodied cognition and tense semantics.

Lack of source memory as a potential marker of early assimilation of novel items into current knowledge.

In daily life, humans process a plethora of new information that can be either consistent (familiar) or inconsistent (novel) with prior knowledge. Over time, both types of information can integrate into our accumulated knowledge base via distinct pathways. However, the mnemonic processes supporting the integration of information that is inconsistent with prior knowledge remain under-characterized. In the current study, we used functional magnetic resonance imaging (fMRI) to examine the initial assimilation of novel items into the semantic network. Participants saw three repetitions of adjective-noun word pairs that were either consistent or inconsistent with prior knowledge. Twenty-four hours later, they were presented with the same stimuli again while undergoing fMRI scans. Outside the scanner, participants completed a surprise recognition test. We found that when the episodic context associated with initially inconsistent items was irretrievable, the neural signature of these items was indistinguishable from that of consistent items. In contrast, initially inconsistent items with accessible episodic contexts showed neural signatures that differed from those associated with consistent items. We suggest that, at least one day post encoding, items inconsistent with prior knowledge can show early assimilation into the semantic network only when their episodic contexts become inaccessible during retrieval, thus evoking a sense of familiarity.

Predictions transform memories: How expected versus unexpected events are integrated or separated in memory.

Our brains constantly generate predictions about the environment based on prior knowledge. Many of the events we experience are consistent with these predictions, while others might be inconsistent with prior knowledge and thus violate our predictions. To guide future behavior, the memory system must be able to strengthen, transform, or add to existing knowledge based on the accuracy of our predictions. We synthesize recent evidence suggesting that when an event is consistent with our predictions, it leads to neural integration between related memories, which is associated with enhanced associative memory, as well as memory biases. Prediction errors, in turn, can promote both neural integration and separation, and lead to multiple mnemonic outcomes. We review these findings and how they interact with factors such as memory reactivation, prediction error strength, and task goals, to offer insight into what determines memory for events that violate our predictions. In doing so, this review brings together recent neural and behavioral research to advance our understanding of how predictions shape memory, and why.

Does this ring a bell? Music-cued retrieval of semantic knowledge and metamemory judgments.

Failed knowledge recall attempts are sometimes accompanied by a strong feeling of imminent success, giving rise to a "tip-of-the-tongue" (TOT) experience. Similar to successful retrieval (i.e., the Know state, K), a TOT commences with strong cue familiarity but involves only partial retrieval of related information. We sought to characterize the cognitive processes and temporal dynamics of these retrieval states and to extend the applicability of previous findings about TOT to the auditory modality. Participants heard 3-sec initial segments of popular songs and were asked to recall their names. EEG was recorded while participants indicated their retrieval state via button press. Stimulus-locked analyses revealed a significant early left fronto-central difference between TOT and K, at 300-550 msec postcue onset. Post hoc analysis revealed that, in this time window, TOT also differed from DK (Don't Know) responses, which themselves were similar to the K responses. This finding indicates that neural processes, which may reflect strategy selection, ease of semantic processing, familiarity-related processes, or conflict monitoring, are indicative of the fate of our knowledge judgments long before we actually execute them.

Putting Humpty together and pulling him apart: accessing and unbinding the hippocampal item-context engram.

A remarkable act of memory entails binding different forms of information. We focus on the timeless question of how the bound engram is accessed such that its component features-item and context-are extracted. To shed light on this question, we investigate the dynamics between brain structures that together mediate the binding and extraction of item and context. Converging evidence has implicated the Parahippocampal cortex (PHc) in contextual processing, the Perirhinal cortex (PRc) in item processing, and the hippocampus in item-context binding. Effective connectivity analysis was conducted on fMRI data gathered during retrieval on tests that differ with regard to the to-be-extracted information. Results revealed that recall is initiated by context-related PHc activity, followed by hippocampal item-context engram activation, and completed with retrieval of the study-item by the PRc. The reverse path was found for recognition. We thus provide novel evidence for dissociative patterns of item-context unbinding during retrieval.

Cooperation between the hippocampus and the striatum during episodic encoding.

The hippocampus and the striatum are thought to play distinct roles in learning and memory, each supporting an independent memory system. A fundamental question is whether, and how, these systems interact to jointly contribute to learning and memory. In particular, it remains unknown whether the striatum contributes selectively to implicit, habitual learning, or whether the striatum may also contribute to long-term episodic memory. Here, we show with functional magnetic resonance imaging (fMRI) that the hippocampus and the striatum interact cooperatively to support episodic memory formation. Participants were scanned during a memory encoding paradigm and, subsequently, were tested for memory of encoded items. fMRI data revealed that successful memory was associated with greater activity in both the hippocampus and the striatum (putamen) during encoding. Furthermore, activity in the hippocampus and the striatum was correlated within subjects for items that were later remembered, but not for items that were forgotten. Finally, across subjects, the strength of the correlation between the hippocampus and the striatum predicted memory success. These findings provide novel evidence for contributions of both the striatum and the hippocampus to successful episodic encoding and for a cooperative interaction between them.

Explicit memory for unattended words: the importance of being in the "no".

Recognition tests in which participants indicate whether they recognize items using binary yes/no response options have typically yielded "yes" responses at equal rates for unattended old items and new items. Because most responses to unattended stimuli in such tests are "no" responses, we reasoned that a closer examination of "no" responses might reveal memory for unattended items. We modified a classic paradigm to allow participants to indicate high and low levels of confidence in their responses. As in earlier studies, the overall proportion of "yes" responses did not differ between unattended old items and new items. However, there was a crossover effect in the "no" responses: More high-confidence "no" responses were given for new items than for unattended old items, whereas more low-confidence "no" responses were given for unattended old items than for new items. These results indicate explicit memory for unattended material presented under high perceptual load. Our findings suggest that the null effects obtained in previous studies may not have stemmed from failures of perception or memory, but rather may have been due to insufficiently sensitive memory assessment.

Examining the transition of novel information toward familiarity.

Throughout their lives, humans encounter multiple instances of new information that can be inconsistent with prior knowledge (novel). Over time, the once-novel information becomes integrated into their established knowledge base, shifting from novelty to familiarity. In this study, we investigated the processes by which the first steps of this transition take place. We hypothesized that the neural representations of initially novel items gradually change over the course of repeated presentations, expressing a shift toward familiarity. We further assumed that this shift could be traced by examining neural patterns using fMRI. In two experiments, while being scanned, participants read noun-adjective word pairs that were either consistent or inconsistent with their prior knowledge. Stimuli were repeated 3-6 times within the scans. Employing mass univariate and multivariate similarity analyses, we showed that the neural representations associated with the initial presentation of familiar versus novel objects differed in lateral frontal and temporal regions, the medial prefrontal cortex, and the medial temporal lobe. Importantly, the neural representations of novel stimuli gradually changed throughout repetitions until they became indistinguishable from their respective familiar items. We interpret these findings as indicating that an early phase of familiarization can be completed within a few repetitions. This initial familiarization can then serve as the prerequisite to the integration of novel items into existing knowledge. Future empirical and theoretical works can build on the current findings to develop a comprehensive model of the transition from novelty to familiarity.

Prior knowledge promotes hippocampal separation but cortical assimilation in the left inferior frontal gyrus.

An adaptive memory system rarely learns information tabula rasa, but rather builds on prior knowledge to facilitate learning. How prior knowledge influences the neural representation of novel associations remains unknown. Here, participants associated pairs of faces in two conditions: a famous, highly familiar face with a novel face or two novel faces while undergoing fMRI. We examine multivoxel activity patterns corresponding to individual faces before and after learning. The activity patterns representing members of famous-novel pairs becomes separated in the hippocampus, that is, more distinct from one another through learning, in striking contrast to paired novel faces that become similar. In the left inferior frontal gyrus, however, prior knowledge leads to integration, and in a specific direction: the representation of the novel face becomes similar to that of the famous face after learning, suggesting assimilation of new into old memories. We propose that hippocampal separation might resolve interference between existing and newly learned information, allowing cortical assimilation. Thus, associative learning with versus without prior knowledge relies on radically different computations.

Distinctiveness Benefits Novelty (and Not Familiarity), but Only Up to a Limit: The Prior Knowledge Perspective.

Novelty is a pivotal player in cognition, and its contribution to superior memory performance is a widely accepted convention. On the other hand, mnemonic advantages for familiar information are also well documented. Here, we examine the role of experimental distinctiveness as a potential explanation for these apparently conflicting findings. Across two experiments, we demonstrate that conceptual novelty, an unfamiliar combination of familiar constituents, is sensitive to its experimental proportions: Improved memory for novelty was observed when novel stimuli were relatively rare. Memory levels for familiar items, in contrast, were completely unaffected by experimental proportions, highlighting their insensitivity to list-based distinctiveness. Finally, no mnemonic advantage for conceptual novelty over familiarity was observed even when novel stimuli were extremely rare at study. Together, these results imply that novel and familiar items are processed via partially distinct mechanisms, with (at least some facets of) novelty not providing a mnemonic advantage over familiarity.

I know I've seen you before: Distinguishing recent-single-exposure-based familiarity from pre-existing familiarity.

This study examines how individuals differentiate recent-single-exposure-based familiarity from pre-existing familiarity. If these are two distinct cognitive processes, are they supported by the same neural bases? This study examines how recent-single-exposure-based familiarity and multiple-previous-exposure-based familiarity are supported and represented in the brain using functional MRI. In a novel approach, we first behaviorally show that subjects can divide retrieval of items in pre-existing memory into judgments of recollection and familiarity. Then, using functional magnetic resonance imaging, we examine the differences in blood oxygen level dependent activity and regional connectivity during judgments of recent-single-exposure-based and pre-existing familiarity. Judgments of these two types of familiarity showed distinct regions of activation in a whole-brain analysis, in medial temporal lobe (MTL) substructures, and in MTL substructure functional-correlations with other brain regions. Specifically, within the MTL, perirhinal cortex showed increased activation during recent-single-exposure-based familiarity while parahippocampal cortex showed increased activation during judgments of pre-existing familiarity. We find that recent-single-exposure-based and pre-existing familiarity are represented as distinct neural processes in the brain; this is supported by differing patterns of brain activation and regional correlations. This spatially distinct regional brain involvement suggests that the two separate experiences of familiarity, recent-exposure-based familiarity and pre-existing familiarity, may be cognitively distinct.

Delineating the effect of semantic congruency on episodic memory: the role of integration and relatedness.

A fundamental challenge in the study of learning and memory is to understand the role of existing knowledge in the encoding and retrieval of new episodic information. The importance of prior knowledge in memory is demonstrated in the congruency effect-the robust finding wherein participants display better memory for items that are compatible, rather than incompatible, with their pre-existing semantic knowledge. Despite its robustness, the mechanism underlying this effect is not well understood. In four studies, we provide evidence that demonstrates the privileged explanatory power of the elaboration-integration account over alternative hypotheses. Furthermore, we question the implicit assumption that the congruency effect pertains to the truthfulness/sensibility of a subject-predicate proposition, and show that congruency is a function of semantic relatedness between item and context words.

From mind to matter: neural correlates of abstract and concrete mindsets.

Much work in the field of social cognition shows that adopting an abstract (vs concrete) mindset alters the way people construe the world, thereby exerting substantial effects across innumerable aspects of human behavior. In order to investigate the cognitive and neural basis of these effects, we scanned participants as they performed two widely used tasks that induce an abstracting vs concretizing mindsets. Specifically, participants: (i) indicated 'why' perform certain activities (a task that involves abstraction) or 'how' the same activities are performed (a task that involves concretization) and (ii) generated superordinate categories for certain objects (a task that involves abstraction) or subordinate exemplars for the same objects (a task that involves concretization). We conducted a conjunction analysis of the two tasks, in order to uncover the neural activity associated with abstraction and concretization. The results showed that concretization was associated with activation in fronto-parietal regions implicated in goal-directed action; abstraction was associated with activity within posterior regions implicated in visual perception. We discuss these findings in light of construal-level theory's notion of abstraction.

Prior knowledge influences on hippocampus and medial prefrontal cortex interactions in subsequent memory.

Prior knowledge is known to influence the encoding of new events. Specifically, recent theoretical frameworks suggest that positively correlated hippocampus (HC)-medial prefrontal cortex (mPFC) activity is involved in creating enduring traces of events inconsistent with our prior knowledge. Events that are consistent with our schemas are suggested to be encoded via mPFC-cortical interactions. Previous studies examined differences in functional connectivity between subsequently remembered and forgotten items, but the source of these differences was not addressed. Therefore, the involvement of the inter-regions functional connectivity in subsequent remembering or subsequent forgetting of events is unknown. In this study, in addition to probing for a remembered-forgotten difference in functional connectivity, we also examined how connectivity differed from baseline in each of the memory conditions. At encoding, the participants were presented with pairs of semantically related (schema-consistent) and semantically unrelated (schema-inconsistent) words. A surprise recognition test was administered, and a subsequent memory analysis evaluating potential interactions with the HC and mPFC was conducted. Consistent with the suggested frameworks, subsequent memory modulated HC-mPFC connectivity only in schema-inconsistent events. Importantly, the HC and mPFC were positively correlated with respect to subsequently remembered schema-inconsistent items, whereas the subsequently forgotten schema-inconsistent events did not differ from baseline. We also found that positively correlated activity of the mPFC with visual and parietal regions mediated subsequent memory of schema-inconsistent items. Therefore, inconsistent events may be encoded by a network of cortical and medial temporal lobe regions.

"I remember thinking ": Neural activity associated with subsequent memory for stimulus-evoked internal mentations.

Conscious thought involves an interpretive inner monologue pertaining to our waking experiences. Previous studies focused on the mechanisms that allow us to remember externally presented stimuli, but the neurobiological basis of the ability to remember one's internal mentations remains unknown. In order to investigate this question, we presented participants with sentences and scanned their neural activity using functional magnetic resonance imaging (fMRI) as they incidentally produced spontaneous internal mentations. After the scan, we presented the sentences again and asked participants to describe the specific thoughts they had during the initial presentation of each sentence. We categorized experimental trials for each participant according to whether they resulted in subsequently reported internal mentations or not. The results show that activation within classic language processing areas was associated with participants' ability to recollect their thoughts. Activation within mostly right lateralized and medial "default-mode network" regions was associated with not reporting such thoughts.

Encoding-related brain activity dissociates between the recollective processes underlying successful recall and recognition: a subsequent-memory study.

The subsequent-memory (SM) paradigm uncovers brain mechanisms that are associated with mnemonic activity during encoding by measuring participants' neural activity during encoding and classifying the encoding trials according to performance in the subsequent retrieval phase. The majority of these studies have converged on the notion that the mechanism supporting recognition is mediated by familiarity and recollection. The process of recollection is often assumed to be a recall-like process, implying that the active search for the memory trace is similar, if not identical, for recall and recognition. Here we challenge this assumption and hypothesize - based on previous findings obtained in our lab - that the recollective processes underlying recall and recognition might show dissociative patterns of encoding-related brain activity. To this end, our design controlled for familiarity, thereby focusing on contextual, recollective processes. We found evidence for dissociative neurocognitive encoding mechanisms supporting subsequent-recall and subsequent-recognition. Specifically, the contrast of subsequent-recognition versus subsequent-recall revealed activation in the Parahippocampal cortex (PHc) and the posterior hippocampus--regions associated with contextual processing. Implications of our findings and their relation to current cognitive models of recollection are discussed.

When two sources of fluency meet one cognitive mindset.

Fluency, the subjective experience of ease associated with information processing, has been shown to affect a host of judgments. Previous research has typically focused on specific factors that affect the use of a single, specific fluency source. In the present study we examine how cognitive mindsets, or processing modes, moderate fluency emanating from two simultaneous sources of fluency. As a cognitive mindset manipulation, participants performed Jacoby's process dissociation paradigm. Subsequently, participants engaged in a metamemory task that incorporates (and can separately measure the influence of) two simultaneous sources of fluency: familiarity and accessibility. Our results confirmed that our content-unrelated mindset procedure had affected the use of fluency. Moreover, the use of both fluency sources was attenuated, demonstrating the generality of the effect. The findings highlight the causal dependency of fluency on a complex, cognitively-rich environment.