Tomatoes Are Red: The Perception of Achromatic Objects Elicits Retrieval of Associated Color Knowledge.

When preparing to name an object, semantic knowledge about the object and its attributes is activated, including perceptual properties. It is unclear, however, whether semantic attribute activation contributes to lexical access or is a consequence of activating a concept irrespective of whether that concept is to be named or not. In this study, we measured neural responses using fMRI while participants named objects that are typically green or red, presented in black line drawings. Furthermore, participants underwent two other tasks with the same objects, color naming and semantic judgment, to see if the activation pattern we observe during picture naming is (a) similar to that of a task that requires accessing the color attribute and (b) distinct from that of a task that requires accessing the concept but not its name or color. We used representational similarity analysis to detect brain areas that show similar patterns within the same color category, but show different patterns across the two color categories. In all three tasks, activation in the bilateral fusiform gyri ("Human V4") correlated with a representational model encoding the red-green distinction weighted by the importance of color feature for the different objects. This result suggests that when seeing objects whose color attribute is highly diagnostic, color knowledge about the objects is retrieved irrespective of whether the color or the object itself have to be named.

Speaking in the Brain: The Interaction between Words and Syntax in Sentence Production.

This neuroimaging study investigated the neural infrastructure of sentence-level language production. We compared brain activation patterns, as measured with BOLD-fMRI, during production of sentences that differed in verb argument structures (intransitives, transitives, ditransitives) and the lexical status of the verb (known verbs or pseudoverbs). The experiment consisted of 30 mini-blocks of six sentences each. Each mini-block started with an example for the type of sentence to be produced in that block. On each trial in the mini-blocks, participants were first given the (pseudo-)verb followed by three geometric shapes to serve as verb arguments in the sentences. Production of sentences with known verbs yielded greater activation compared to sentences with pseudoverbs in the core language network of the left inferior frontal gyrus, the left posterior middle temporal gyrus, and a more posterior middle temporal region extending into the angular gyrus, analogous to effects observed in language comprehension. Increasing the number of verb arguments led to greater activation in an overlapping left posterior middle temporal gyrus/angular gyrus area, particularly for known verbs, as well as in the bilateral precuneus. Thus, producing sentences with more complex structures using existing verbs leads to increased activation in the language network, suggesting some reliance on memory retrieval of stored lexical-syntactic information during sentence production. This study thus provides evidence from sentence-level language production in line with functional models of the language network that have so far been mainly based on single-word production, comprehension, and language processing in aphasia.

Mindwandering propensity modulates episodic memory consolidation.

Research into strategies that can combat episodic memory decline in healthy older adults has gained widespread attention over the years. Evidence suggests that a short period of rest immediately after learning can enhance memory consolidation, as compared to engaging in cognitive tasks. However, a recent study in younger adults has shown that post-encoding engagement in a working memory task leads to the same degree of memory consolidation as from post-encoding rest. Here, we tested whether this finding can be extended to older adults. Using a delayed recognition test, we compared the memory consolidation of word-picture pairs learned prior to 9 min of rest or a 2-Back working memory task, and examined its relationship with executive functioning and mindwandering propensity. Our results show that (1) similar to younger adults, memory for the word-picture associations did not differ when encoding was followed by post-encoding rest or 2-Back task and (2) older adults with higher mindwandering propensity retained more word-picture associations encoded prior to rest relative to those encoded prior to the 2-Back task, whereas participants with lower mindwandering propensity had better memory performance for the pairs encoded prior to the 2-Back task. Overall, our results indicate that the degree of episodic memory consolidation during both active and passive post-encoding periods depends on individual mindwandering tendency.

Theta-band Oscillations in the Middle Temporal Gyrus Reflect Novel Word Consolidation.

Like many other types of memory formation, novel word learning benefits from an offline consolidation period after the initial encoding phase. A previous EEG study has shown that retrieval of novel words elicited more word-like-induced electrophysiological brain activity in the theta band after consolidation [Bakker, I., Takashima, A., van Hell, J. G., Janzen, G., & McQueen, J. M. Changes in theta and beta oscillations as signatures of novel word consolidation. Journal of Cognitive Neuroscience, 27, 1286-1297, 2015]. This suggests that theta-band oscillations play a role in lexicalization, but it has not been demonstrated that this effect is directly caused by the formation of lexical representations. This study used magnetoencephalography to localize the theta consolidation effect to the left posterior middle temporal gyrus (pMTG), a region known to be involved in lexical storage. Both untrained novel words and words learned immediately before test elicited lower theta power during retrieval than existing words in this region. After a 24-hr consolidation period, the difference between novel and existing words decreased significantly, most strongly in the left pMTG. The magnitude of the decrease after consolidation correlated with an increase in behavioral competition effects between novel words and existing words with similar spelling, reflecting functional integration into the mental lexicon. These results thus provide new evidence that consolidation aids the development of lexical representations mediated by the left pMTG. Theta synchronization may enable lexical access by facilitating the simultaneous activation of distributed semantic, phonological, and orthographic representations that are bound together in the pMTG.

The dynamics of memory consolidation of landmarks.

Navigating through space is fundamental to human nature and requires the ability to retrieve relevant information from the remote past. With the passage of time, some memories become generic, capturing only a sense of familiarity. Yet, others maintain precision, even when acquired decades ago. Understanding the dynamics of memory consolidation is a major challenge to neuroscientists. Using functional magnetic resonance imaging, we systematically examined the effects of time and spatial context on the neural representation of landmark recognition memory. An equal number of male and female subjects (males N = 10, total N = 20) watched a route through a large-scale virtual environment. Landmarks occurred at navigationally relevant and irrelevant locations along the route. Recognition memory for landmarks was tested directly following encoding, 24 h later and 30 days later. Surprisingly, changes over time in the neural representation of navigationally relevant landmarks differed between males and females. In males, relevant landmarks selectively engaged the parahippocampal gyrus (PHG) regardless of the age of the memory. In females, the response to relevant landmarks gradually diminished with time in the PHG but strengthened progressively in the inferior frontal gyrus (IFG). Based on what is known about the functioning of the PHG and IFG, the findings of this study suggest that males maintain access to the initially formed spatial representation of landmarks whereas females become strongly dependent on a verbal representation of landmarks with time. Our findings yield a clear objective for future studies. © 2017 Wiley Periodicals, Inc.

Repetition Suppression in the Left Inferior Frontal Gyrus Predicts Tone Learning Performance.

Do individuals differ in how efficiently they process non-native sounds? To what extent do these differences relate to individual variability in sound-learning aptitude? We addressed these questions by assessing the sound-learning abilities of Dutch native speakers as they were trained on non-native tone contrasts. We used fMRI repetition suppression to the non-native tones to measure participants' neuronal processing efficiency before and after training. Although all participants improved in tone identification with training, there was large individual variability in learning performance. A repetition suppression effect to tone was found in the bilateral inferior frontal gyri (IFGs) before training. No whole-brain effect was found after training; a region-of-interest analysis, however, showed that, after training, repetition suppression to tone in the left IFG correlated positively with learning. That is, individuals who were better in learning the non-native tones showed larger repetition suppression in this area. Crucially, this was true even before training. These findings add to existing evidence that the left IFG plays an important role in sound learning and indicate that individual differences in learning aptitude stem from differences in the neuronal efficiency with which non-native sounds are processed.

Retrieved emotional context influences hippocampal involvement during recognition of neutral memories.

It is well documented that emotionally arousing experiences are better remembered than mundane events. This is thought to occur through hippocampus-amygdala crosstalk during encoding, consolidation, and retrieval. Here we investigated whether emotional events (context) also cause a memory benefit for simultaneously encoded non-arousing contents and whether this effect persists after a delay via recruitment of a similar hippocampus-amygdala network. Participants studied neutral pictures (content) encoded together with either an arousing or a neutral sound (that served as context) in two study sessions three days apart. Memory was tested in a functional magnetic resonance scanner directly after the second study session. Pictures recognised with high confidence were more often thought to have been associated with an arousing than with a neutral context, irrespective of the veridical source memory. If the retrieved context was arousing, an area in the hippocampus adjacent to the amygdala exhibited heightened activation and this area increased functional connectivity with the parahippocampal gyrus, an area known to process pictures of scenes. These findings suggest that memories can be shaped by the retrieval act. Memory structures may be recruited to a higher degree when an arousing context is retrieved, and this may give rise to confident judgments of recognition for neutral pictures even after a delay.

Transient relay function of midline thalamic nuclei during long-term memory consolidation in humans.

To test the hypothesis that thalamic midline nuclei play a transient role in memory consolidation, we reanalyzed a prospective functional MRI study, contrasting recent and progressively more remote memory retrieval. We revealed a transient thalamic connectivity increase with the hippocampus, the medial prefrontal cortex (mPFC), and a parahippocampal area, which decreased with time. In turn, mPFC-parahippocampal connectivity increased progressively. These findings support a model in which thalamic midline nuclei serve as a hub linking hippocampus, mPFC, and posterior representational areas during memory retrieval at an early (2 h) stage of consolidation, extending classical systems consolidation models by attributing a transient role to midline thalamic nuclei.

Changes in theta and beta oscillations as signatures of novel word consolidation.

The complementary learning systems account of word learning states that novel words, like other types of memories, undergo an offline consolidation process during which they are gradually integrated into the neocortical memory network. A fundamental change in the neural representation of a novel word should therefore occur in the hours after learning. The present EEG study tested this hypothesis by investigating whether novel words learned before a 24-hr consolidation period elicited more word-like oscillatory responses than novel words learned immediately before testing. In line with previous studies indicating that theta synchronization reflects lexical access, unfamiliar novel words elicited lower power in the theta band (4-8 Hz) than existing words. Recently learned words still showed a marginally lower theta increase than existing words, but theta responses to novel words that had been acquired 24 hr earlier were indistinguishable from responses to existing words. Consistent with evidence that beta desynchronization (16-21 Hz) is related to lexical-semantic processing, we found that both unfamiliar and recently learned novel words elicited less beta desynchronization than existing words. In contrast, no difference was found between novel words learned 24 hr earlier and existing words. These data therefore suggest that an offline consolidation period enables novel words to acquire lexically integrated, word-like neural representations.

Memory stabilization with targeted reactivation during human slow-wave sleep.

It is believed that neural representations of recent experiences become reactivated during sleep, and that this process serves to stabilize associated memories in long-term memory. Here, we initiated this reactivation process for specific memories during slow-wave sleep. Participants studied 50 object-location associations with object-related sounds presented concurrently. For half of the associations, the related sounds were re-presented during subsequent slow-wave sleep while participants underwent functional MRI. Compared with control sounds, related sounds were associated with increased activation of right parahippocampal cortex. Postsleep memory accuracy was positively correlated with sound-related activation during sleep in various brain regions, including the thalamus, bilateral medial temporal lobe, and cerebellum. In addition, postsleep memory accuracy was also positively correlated with pre- to postsleep changes in parahippocampal-medial prefrontal connectivity during retrieval of reactivated associations. Our results suggest that the brain is differentially activated by studied and unstudied sounds during deep sleep and that the thalamus and medial temporal lobe are involved in establishing the mnemonic consequences of externally triggered reactivation of associative memories.

Neural mechanisms supporting the extraction of general knowledge across episodic memories.

General knowledge acquisition entails the extraction of statistical regularities from the environment. At high levels of complexity, this may involve the extraction, and consolidation, of associative regularities across event memories. The underlying neural mechanisms would likely involve a hippocampo-neocortical dialog, as proposed previously for system-level consolidation. To test these hypotheses, we assessed possible differences in consolidation between associative memories containing cross-episodic regularities and unique associative memories. Subjects learned face-location associations, half of which responded to complex regularities regarding the combination of facial features and locations, whereas the other half did not. Importantly, regularities could only be extracted over hippocampus-encoded, associative aspects of the items. Memory was assessed both immediately after encoding and 48 h later, under fMRI acquisition. Our results suggest that processes related to system-level reorganization occur preferentially for regular associations across episodes. Moreover, the build-up of general knowledge regarding regular associations appears to involve the coordinated activity of the hippocampus and mediofrontal regions. The putative cross-talk between these two regions might support a mechanism for regularity extraction. These findings suggest that the consolidation of cross-episodic regularities may be a key mechanism underlying general knowledge acquisition.

Richness of information about novel words influences how episodic and semantic memory networks interact during lexicalization.

The complementary learning systems account of declarative memory suggests two distinct memory networks, a fast-mapping, episodic system involving the hippocampus, and a slower semantic memory system distributed across the neocortex in which new information is gradually integrated with existing representations. In this study, we investigated the extent to which these two networks are involved in the integration of novel words into the lexicon after extensive learning, and how the involvement of these networks changes after 24h. In particular, we explored whether having richer information at encoding influences the lexicalization trajectory. We trained participants with two sets of novel words, one where exposure was only to the words' phonological forms (the form-only condition), and one where pictures of unfamiliar objects were associated with the words' phonological forms (the picture-associated condition). A behavioral measure of lexical competition (indexing lexicalization) indicated stronger competition effects for the form-only words. Imaging (fMRI) results revealed greater involvement of phonological lexical processing areas immediately after training in the form-only condition, suggesting that tight connections were formed between novel words and existing lexical entries already at encoding. Retrieval of picture-associated novel words involved the episodic/hippocampal memory system more extensively. Although lexicalization was weaker in the picture-associated condition, overall memory strength was greater when tested after a 24hour delay, probably due to the availability of both episodic and lexical memory networks to aid retrieval. It appears that, during lexicalization of a novel word, the relative involvement of different memory networks differs according to the richness of the information about that word available at encoding.

Do testing effects change over time? Insights from immediate and delayed retrieval speed.

Retrieving information from memory improves recall accuracy more than continued studying, but this testing effect often only becomes visible over time. In contrast, the present study documents testing effects on recall speed both immediately after practice and after a delay. A total of 40 participants learned the translation of 100 Swahili words and then further restudied the words with translations or retrieved the translations from memory during testing. As in previous experiments, recall accuracy was higher for restudied words than for tested words immediately after practice, but higher for tested words after 7 days. Response times for correct answers, however, showed a different result: Learners were faster to recall tested words than restudied words both immediately after practice and after 7 days. These results are interpreted in light of recent suggestions that testing selectively strengthens cue-response associations. An additional outcome was that testing effects on recall accuracy were related to perceived retrieval success during practice. When several practice retrievals were successful, testing effects on recall accuracy were already significant immediately after practice. Together with the reaction time data, this supports recent models that attribute changes in testing effects over time to limited item retrievability during practice.

White matter connectivity linked to novel word learning in children.

Children and adults are excellent word learners. Increasing evidence suggests that the neural mechanisms that allow us to learn words change with age. In a recent fMRI study from our group, several brain regions exhibited age-related differences when accessing newly learned words in a second language (L2; Takashima et al. Dev Cogn Neurosci 37, 2019). Namely, while the Teen group (aged 14-16 years) activated more left frontal and parietal regions, the Young group (aged 8-10 years) activated right frontal and parietal regions. In the current study we analyzed the structural connectivity data from the aforementioned study, examining the white matter connectivity of the regions that showed age-related functional activation differences. Age group differences in streamline density as well as correlations with L2 word learning success and their interaction were examined. The Teen group showed stronger connectivity than the Young group in the right arcuate fasciculus (AF). Furthermore, white matter connectivity and memory for L2 words across the two age groups correlated in the left AF and the right anterior thalamic radiation (ATR) such that higher connectivity in the left AF and lower connectivity in the right ATR was related to better memory for L2 words. Additionally, connectivity in the area of the right AF that exhibited age-related differences predicted word learning success. The finding that across the two age groups, stronger connectivity is related to better memory for words lends further support to the hypothesis that the prolonged maturation of the prefrontal cortex, here in the form of structural connectivity, plays an important role in the development of memory.

Neural correlates of testing effects in vocabulary learning.

Tests that require memory retrieval strongly improve long-term retention in comparison to continued studying. For example, once learners know the translation of a word, restudy practice, during which they see the word and its translation again, is less effective than testing practice, during which they see only the word and retrieve the translation from memory. In the present functional magnetic resonance imaging (fMRI) study, we investigated the neuro-cognitive mechanisms underlying this striking testing effect. Twenty-six young adults without prior knowledge of Swahili learned the translation of 100 Swahili words and then further practiced the words in an fMRI scanner by restudying or by testing. Recall of the translations on a final memory test after one week was significantly better and faster for tested words than for restudied words. Brain regions that were more active during testing than during restudying included the left inferior frontal gyrus, ventral striatum, and midbrain areas. Increased activity in the left inferior parietal and left middle temporal areas during testing but not during restudying predicted better recall on the final memory test. Together, results suggest that testing may be more beneficial than restudying due to processes related to targeted semantic elaboration and selective strengthening of associations between retrieval cues and relevant responses, and may involve increased effortful cognitive control and modulations of memory through striatal motivation and reward circuits.

The neocortical network representing associative memory reorganizes with time in a process engaging the anterior temporal lobe.

During encoding, the distributed neocortical representations of memory components are presumed to be associatively linked by the hippocampus. With time, a reorganization of brain areas supporting memory takes place, which can ultimately result in memories becoming independent of the hippocampus. While it is theorized that with time, the neocortical representations become linked by higher order neocortical association areas, this remains to be experimentally supported. In this study, 24 human participants encoded sets of face-location associations, which they retrieved 1 or 25 h later ("recent" and "remote" conditions, respectively), while their brain activity was recorded using whole-head magnetoencephalography. We investigated changes in the functional interactions between the neocortical representational areas emerging over time. To assess functional interactions, trial-by-trial high gamma (60-140 Hz) power correlations were calculated between the neocortical representational areas relevant to the encoded information, namely the fusiform face area (FFA) and posterior parietal cortex (PPC). With time, both the FFA and the PPC increased their functional interactions with the anterior temporal lobe (ATL). Given that the ATL is involved in semantic representation of paired associates, our results suggest that, already within 25 h after acquiring new memory associations, neocortical functional links are established via higher order semantic association areas.

Functional neuroanatomy of lexical access in contextually and visually guided spoken word production.

Lexical access is commonly studied using bare picture naming, which is visually guided, but in real-life conversation, lexical access is more commonly contextually guided. In this fMRI study, we examined the underlying functional neuroanatomy of contextually and visually guided lexical access, and its consistency across sessions. We employed a context-driven picture naming task with fifteen healthy speakers reading incomplete sentences (word-by-word) and subsequently naming the picture depicting the final word. Sentences provided either a constrained or unconstrained lead-in setting for the picture to be named, thereby approximating lexical access in natural language use. The picture name could be planned either through sentence context (constrained) or picture appearance (unconstrained). This procedure was repeated in an equivalent second session two to four weeks later with the same sample to test for test-retest consistency. Picture naming times showed a strong context effect, confirming that constrained sentences speed up production of the final word depicted as an image. fMRI results showed that the areas common to contextually and visually guided lexical access were left fusiform and left inferior frontal gyrus (both consistently active across-sessions), and middle temporal gyrus. However, non-overlapping patterns were also found, notably in the left temporal and parietal cortices, suggesting a different neural circuit for contextually versus visually guided lexical access.

Functional connectivity during light sleep is correlated with memory performance for face-location associations.

The consolidation of declarative memories benefits from sleep. The neural mechanisms involved in sleep-dependent consolidation, however, are largely unknown. Here, we used a combination of functional magnetic resonance imaging, polysomnography and a face-location associative memory task to target neural connectivity of a face sensitive area during an afternoon nap. Fusiform connectivity was substantially greater during sleep stage 1 than in wake in a network extending from early visual areas bilaterally to the fusiform gyrus, ventrally and into the posterior parietal cortices, dorsally. In sleep stage 2, fusiform connectivity was found to be larger in the precuneus, bilateral middle temporal gyrus and medial prefrontal cortex. Specific functional connectivity increases observed during light sleep were positively correlated with memory performance for face-location associations. A distinction could be made between fusiform-medial prefrontal connectivity during sleep stage 1 and 2 that was positively correlated with retention of associations learned prior to sleep and fusiform-hippocampal connectivity during sleep stage 1 that was correlated with better acquisition of new associations learned after sleep. Our results suggest that fusiform-medial prefrontal connectivity during sleep has a stabilizing effect on recently learned associative memories, possibly due to the existence of a task-related schema that allows rapid consolidation of related information. Our data further indicate that sleep-dependent connectivity between the fusiform gyrus and hippocampus correlated with new learning after sleep. Thus, our study provides correlational evidence for the behavioral relevance of specific medial prefrontal and hippocampal interactions with the fusiform gyrus during light sleep.

Increase in posterior alpha activity during rehearsal predicts successful long-term memory formation of word sequences.

It is becoming increasingly clear that demanding cognitive tasks rely on an extended network engaging task-relevant areas and, importantly, disengaging task-irrelevant areas. Given that alpha activity (8-12 Hz) has been shown to reflect the disengagement of task-irrelevant regions in attention and working memory tasks, we here ask if alpha activity plays a related role for long-term memory formation. Subjects were instructed to encode and maintain the order of word sequences while the ongoing brain activity was recorded using magnetoencephalography (MEG). In each trial, three words were presented followed by a 3.4 s rehearsal interval. Considering the good temporal resolution of MEG this allowed us to investigate the word presentation and rehearsal interval separately. The sequences were grouped in trials where word order either could be tested immediately (working memory trials; WM) or later (LTM trials) according to instructions. Subjects were tested on their ability to retrieve the order of the three words. The data revealed that alpha power in parieto-occipital regions was lower during word presentation compared to rehearsal. Our key finding was that parieto-occipital alpha power during the rehearsal period was markedly stronger for successfully than unsuccessfully encoded LTM sequences. This subsequent memory effect demonstrates that high posterior alpha activity creates an optimal brain state for successful LTM formation possibly by actively reducing parieto-occipital activity that might interfere with sequence encoding.

Shift from hippocampal to neocortical centered retrieval network with consolidation.

The standard model of system-level consolidation posits that the hippocampus is part of a retrieval network for recent memories. According to this theory, the memories are gradually transferred to neocortical circuits with consolidation, where the connections within this circuit grow stronger and reorganized so that redundant and/or contextual details may be lost. Thus, remote memories are based on neocortical networks and can be retrieved independently of the hippocampus. To test this model, we measured regional brain activity and connectivity during retrieval with functional magnetic resonance imaging. Subjects were trained on two sets of face-location association and were tested with two different delays, 15 min and 24 h including a whole night of sleep. We hypothesized that memory traces of the locations associated with specific faces will be linked through the hippocampus for the retrieval of recently learned association, but with consolidation, the activity and the functional connectivity between the neocortical areas will increase. We show that posterior hippocampal activity related to high-confidence retrieval decreased and neocortical activity increased with consolidation. Moreover, the connectivity between the hippocampus and the neocortical regions decreased and in turn, cortico-cortical connectivity between the representational areas increased. The results provide mechanistic support for a two-level process of the declarative memory system, involving initial representation of new associations in a network including the hippocampus and subsequent consolidation into a predominantly neocortical network.