Left Posterior Parietal Cortex Participates in Both Task Preparation and Episodic Retrieval

Optimal memory retrieval depends not only on the fidelity of stored information, but also on the attentional state of the subject. Factors such as mental preparedness to engage in stimulus processing can facilitate or hinder memory retrieval. The current study used functional magnetic resonance imaging (fMRI) to distinguish preparatory brain activity before episodic and semantic retrieval tasks from activity associated with retrieval itself. The use of a catch-trial imaging paradigm permitted separation of neural responses to preparatory task cues and memory probes. Episodic and semantic task preparation engaged a common network, including the bilateral intraparietal sulcus (IPS), left fusiform gyrus (FFG), and pre-SMA. In the subsequent retrieval phase, the left IPS participated in a frontoparietal network which responded differentially to old and new stimuli. In contrast, the right IPS was influenced only by preparatory cues, with minimal modulation during memory retrieval. Preparatory activity in the left IPS and its sensitivity to old/new differences indicate that this brain region participates both in task preparation and in episodic retrieval. This dual response profile suggests the left IPS as a possible interface between systems for domain-general attentional control and episodic retrieval

Modulation of Oscillatory Power and Connectivity in the Human Posterior Cingulate Cortex Supports the Encoding and Retrieval of Episodic Memories

Existing data from noninvasive studies have led researchers to posit that the posterior cingulate cortex (PCC) supports mnemonic processes: It exhibits degeneration in memory disorders, and fMRI investigations have demonstrated memory-related activation principally during the retrieval of memory items. Despite these data, the role of the PCC in episodic memory has received only limited treatment using the spatial and temporal precision of intracranial EEG, with previous analyses focused on item retrieval. Using data gathered from 21 human participants who underwent stereo-EEG for seizure localization, we characterized oscillatory patterns in the PCC during the encoding and retrieval of episodic memories. We identified a subsequent memory effect during item encoding characterized by increased gamma band oscillatory power and a low-frequency power desynchronization. Fourteen participants had stereotactic electrodes located simultaneously in the hippocampus and PCC, and with these unique data, we describe connectivity changes between these structures that predict successful item encoding and that precede item retrieval. Oscillatory power during retrieval matched the pattern we observed during encoding, with low-frequency (below 15 Hz) desynchronization and a gamma band (especially high gamma, 70–180 Hz) power increase. Encoding is characterized by synchrony between the hippocampus and PCC, centered at 3 Hz, consistent with other observations of properties of this oscillation akin to those for rodent theta activity. We discuss our findings in light of existing theories of episodic memory processing, including the information via desynchronization hypothesis and retrieved context theory, and examine how our data fit with existing theories for the functional role of the PCC. These include a postulated role for the PCC in modulating internally directed attention and for representing or integrating contextual information for memory items

Impact of Load-Related Neural Processes on Feature Binding in Visuospatial Working Memory

BACKGROUND: The capacity of visual working memory (WM) is substantially limited and only a fraction of what we see is maintained as a temporary trace. The process of binding visual features has been proposed as an adaptive means of minimising information demands on WM. However the neural mechanisms underlying this process, and its modulation by task and load effects, are not well understood. OBJECTIVE: To investigate the neural correlates of feature binding and its modulation by WM load during the sequential phases of encoding, maintenance and retrieval. METHODS AND FINDINGS: 18 young healthy participants performed a visuospatial WM task with independent factors of load and feature conjunction (object identity and position) in an event-related functional MRI study. During stimulus encoding, load-invariant conjunction-related activity was observed in left prefrontal cortex and left hippocampus. During maintenance, greater activity for task demands of feature conjunction versus single features, and for increased load was observed in left-sided regions of the superior occipital cortex, precuneus and superior frontal cortex. Where these effects were expressed in overlapping cortical regions, their combined effect was additive. During retrieval, however, an interaction of load and feature conjunction was observed. This modulation of feature conjunction activity under increased load was expressed through greater deactivation in medial structures identified as part of the default mode network. CONCLUSIONS AND SIGNIFICANCE: The relationship between memory load and feature binding qualitatively differed through each phase of the WM task. Of particular interest was the interaction of these factors observed within regions of the default mode network during retrieval which we interpret as suggesting that at low loads, binding processes may be 'automatic' but at higher loads it becomes a resource-intensive process leading to disengagement of activity in this network. These findings provide new insights into how feature binding operates within the capacity-limited WM system

Functional MRI and behavioral investigations of long-term memory-guided visuospatial attention

Real-world human visual perception is superb, despite pervasive attentional capacity limitations that can severely impact behavioral performance. Long-term memory (LTM) is suggested to play a key role in efficiently deploying attentional resources; however, the nature of LTM-attention interactions remains poorly understood. Here, I present a series of behavioral and functional magnetic resonance imaging (fMRI) investigations of the mechanisms of LTM-guided visual attention in 139 healthy participants (18-34 years). In Experiment 1, I hypothesized that humans can use memory to guide spatial attention to multiple discrete locations that have been previously studied. Participants were able to simultaneously attend to more than one spatial location using an LTM cue in a novel change-detection behavioral paradigm also used in fMRI Experiments 2 and 4. Cortical networks associated with LTM and attention often interact competitively. In Experiment 2, I hypothesized that the cognitive control network supports cooperation between LTM and attention. Three posterior regions involved with cognitive control were more strongly recruited for LTM-guided attention than stimulus-guided attention: the posterior precuneus, posterior callosal sulcus, and lateral intraparietal sulcus. In Experiment 3, I hypothesized that regions identified in Experiment 2 are specifically activated for LTM-guided attention, not for LTM retrieval or stimulus-guided attention alone. This hypothesis was supported. Taken together, the results of Experiments 2 and 3 identify a cognitive control subnetwork specifically recruited for LTM-guided attention. Experiment 4 tested how LTM-guided attention affected spatial responsivity of maps within intraparietal sulcus. I hypothesized that left parietal maps would change their spatial responsivity due to the left lateralized effects of memory retrieval. During stimulus-guided attention, contralateral visuotopic maps in the right but not left intraparietal sulcus responded to the full visual field. In contrast, during LTM-guided attention, maps in both the left and right intraparietal sulcus responded to the full visual field, providing evidence for complementary forms of dynamic recruitment under different attentional conditions. Together, these results demonstrate that LTM-guided attention is supported by a parietal subnetwork within the cognitive control network and that internal attentional states influence the spatial specificity of visuotopically mapped regions in parietal cortex

Recurrent Activity in Higher Order, Modality Non-Specific Brain Regions: A Granger Causality Analysis of Autobiographic Memory Retrieval

It has been proposed that the workings of the brain are mainly intrinsically generated recurrent neuronal activity, with sensory inputs as modifiers of such activity in both sensory and higher order modality non-specific regions. This is supported by the demonstration of recurrent neuronal activity in the visual system as a response to visual stimulation. In contrast recurrent activity has never been demonstrated before in higher order modality non-specific regions. Using magneto-encephalography and Granger causality analysis, we tested in a paralimbic network the hypothesis that stimulation may enhance causal recurrent interaction between higher-order, modality non-specific regions. The network includes anterior cingulate/medial prefrontal and posterior cingulate/medial parietal cortices together with pulvinar thalami, a network known to be effective in autobiographic memory retrieval and self-awareness. Autobiographic memory retrieval of previous personal judgments of visually presented words was used as stimuli. It is demonstrated that the prestimulus condition is characterized by causal, recurrent oscillations which are maximal in the lower gamma range. When retrieving previous judgments of visually presented adjectives, this activity is dramatically increased during the stimulus task as ascertained by Granger causality analysis. Our results confirm the hypothesis that stimulation may enhance causal interaction between higher order, modality non-specific brain regions, exemplified in a network of autobiographical memory retrieval

Long-term memory encoding of facial information in humans: an EEG and tACS study

In recent years, the investigation of memory formation and retrieval has attracted increasing interest. As oscillatory activity plays a crucial role in neuroplastic processes, episodic memory is to a considerable extent attributable to synaptic changes, synchronization, and neurophysiological alterations through oscillating electric fields. Perception processes are part of episodic memory encoding. Human face perception and encoding arouse particular interest due to their fundamental relevance in social behavior. This study aimed to determine the causal role of brain dynamics in the encoding of facial episodic memory in humans. As recent studies revealed an enhancement in cognitive processes by the entrainment of internal brain oscillations, tACS stepped up as a new method of non-invasive brain stimulation to induce neuroplasticity (Antal et al. 2008; Antal and Herrmann 2016). It is a promising tool to test the role of brain oscillations on episodic memory encoding in humans and the potential for memory improvement. For the entire study, we developed a memory task that includes encoding, a Short-Term Memory Retrieval Part, maintenance, and a Long-Term Memory Retrieval Part. In the longterm face recognition, we assessed both the performance and the choice confidence on the 3-point scale. Two consecutive experiments were performed. For the first experiment (20 participants), we used 128-channel EEG to identify the region of the brain that is exclusively responsible for the long-term face encoding and the frequency of the brain rhythm that is associated with the successful subsequent recognition. Then, we conducted the tACS experiment (25 participants) based on the frequency and spatial data from the EEG experiment. We implemented a double-blinded, randomized, counterbalanced, crossover, and placebo-controlled study design. 20 minutes of 4 Hz-tACS at 3 mA peak-to-peak were applied during the encoding task to the identified right or to the left TPO area for active control. One more session included sham stimulation to one or the other area. The EEG study revealed a significant synchronization of brain oscillations during successful long-term facial memory encoding in the right TPO area at the low theta range (4 Hz). In complete agreement, the placebo-controlled tACS study showed a significant enhancement of long-term memory recognition performance after the low theta-stimulation of the right but not the left TPO area. The results indicate that low theta oscillations in the right TPO area are vital for successful episodic long-term memory encoding of facial stimuli. Secondly, we confirm that active low theta-tACS applied on this area during encoding improves the subsequent memory recognition performance. This supports the concept of lateralization for face processing in the right posterior brain region; moreover it puts forward this area as a crucial neocortical node in communication with the hippocampus for the long-term memory encoding (Pitcher et al. 2011; Geib et al. 2017). The results are in agreement with other studies that revealed a positive correlation between theta power and memory performance (Pahor and Jaušovec 2014; Clouter et al. 2017). However, the present work reveals a causal link between the empowered low theta in the right TPO area and enhanced subsequent long-term memory recognition. In summary, tACS is a highly suitable non-invasive tool to entrain local neocortical low theta activity and enhance long-term memory encoding, which is important in the clinical context for revealing novel therapeutic strategies in prosopagnosia and prosopamnesia.2021-09-1

Individual Differences and Episodic Memory: Examining Behaviour, Genetics, and Brain Activity.

Dual-process models propose that two processes support recognition memory; familiarity, a general sense that something has been previously encountered; and recollection, the retrieval of details concerning the context in which a previous encounter occurred. Event-related potential (ERP) studies of recognition memory have identified a set of old/new effects that are thought to reflect these processes: the 300-500ms bilateral-frontal effect, thought to reflect familiarity and the 500-800ms left-parietal effect, thought to reflect recollection. Whilst the exact functional role of these effects remains unclear, they are widely viewed as reliable indices of retrieval. The ERP literature reviewed in this thesis suggests that the characteristics of these recognition effects vary with task specific details and individual participant differences, suggesting that the recognition effects purported to index retrieval may be conditional on both task and participant. This thesis examined the influence of individual differences on behavioural measures of recognition and the neural correlates of recognition memory, focusing on factors of stimulus material, task performance and participant genotype. Clear evidence of stimulus differences were found, with pictures eliciting more anteriorly distributed effects than words, and a late onsetting frontopolar old/new effect that was unique for voices. Furthermore, the pattern of ERP activity associated with successful recognition of faces appeared to vary as a function of general face recognition ability, with participants poorer at remembering faces exhibiting a 300-500ms old/new effect not present for those good at remembering faces. The data also suggested that activity over right-frontal electrodes, evident in some previous studies, may be participant specific and could reflect additional retrieval support processes. Contrary to expectations, behavioural task performance was not found to significantly modulate the ‘typical’ recognition memory effects. However, a number of genetic polymorphisms were found to significantly influence both behavioural scores and the pattern of ERP activity associated with recognition memory. These results therefore suggest that inherent participant differences influence the neural correlates of recognition memory, in a way that variations in task performance do not. Overall, the results from this thesis therefore suggest that the ‘typical’ bilateral-frontal and left-parietal effects thought to index retrieval are not universal. Furthermore the results suggest that the specific processes engaged during retrieval (as indexed by variations in ERP activity) may be dependent on specific task requirements, stimulus material and the genetic makeup of the individual

Remembering Forward: Neural Correlates of Memory and Prediction in Human Motor Adaptation

We used functional MR imaging (FMRI), a robotic manipulandum and systems identification techniques to examine neural correlates of predictive compensation for spring-like loads during goal-directed wrist movements in neurologically-intact humans. Although load changed unpredictably from one trial to the next, subjects nevertheless used sensorimotor memories from recent movements to predict and compensate upcoming loads. Prediction enabled subjects to adapt performance so that the task was accomplished with minimum effort. Population analyses of functional images revealed a distributed, bilateral network of cortical and subcortical activity supporting predictive load compensation during visual target capture. Cortical regions – including prefrontal, parietal and hippocampal cortices – exhibited trial-by-trial fluctuations in BOLD signal consistent with the storage and recall of sensorimotor memories or “states” important for spatial working memory. Bilateral activations in associative regions of the striatum demonstrated temporal correlation with the magnitude of kinematic performance error (a signal that could drive reward-optimizing reinforcement learning and the prospective scaling of previously learned motor programs). BOLD signal correlations with load prediction were observed in the cerebellar cortex and red nuclei (consistent with the idea that these structures generate adaptive fusimotor signals facilitating cancelation of expected proprioceptive feedback, as required for conditional feedback adjustments to ongoing motor commands and feedback error learning). Analysis of single subject images revealed that predictive activity was at least as likely to be observed in more than one of these neural systems as in just one. We conclude therefore that motor adaptation is mediated by predictive compensations supported by multiple, distributed, cortical and subcortical structures

Spectral parameters modulation and source localization of blink-related alpha and low-beta oscillations differentiate minimally conscious state from vegetative state/unresponsive wakefulness syndrome

Recently, the cortical source of blink-related delta oscillations (delta BROs) in resting healthy subjects has been localized in the posterior cingulate cortex/precuneus (PCC/PCu), one of the main core-hubs of the default-mode network. This has been interpreted as the electrophysiological signature of the automatic monitoring of the surrounding environment while subjects are immersed in self-reflecting mental activities. Although delta BROs were directly correlated to the degree of consciousness impairment in patients with disorders of consciousness, they failed to differentiate vegetative state/unresponsive wakefulness syndrome (VS/UWS) from minimally conscious state (MCS). In the present study, we have extended the analysis of BROs to frequency bands other than delta in the attempt to find a biological marker that could support the differential diagnosis between VS/UWS and MCS. Four patients with VS/UWS, 5 patients with MCS, and 12 healthy matched controls (CTRL) underwent standard 19-channels EEG recordings during resting conditions. Three-second-lasting EEG epochs centred on each blink instance were submitted to time-frequency analyses in order to extract the normalized Blink-Related Synchronization/Desynchronization (nBRS/BRD) of three bands of interest (low-alpha, high-alpha and low-beta) in the time-window of 50-550 ms after the blink-peak and to estimate the corresponding cortical sources of electrical activity. VS/UWS nBRS/BRD levels of all three bands were lower than those related to both CTRL and MCS, thus enabling the differential diagnosis between MCS and VS/UWS. Furthermore, MCS showed an intermediate signal intensity on PCC/PCu between CTRL and VS/UWS and a higher signal intensity on the left temporo-parieto-occipital junction and inferior occipito-temporal regions when compared to VS/UWS. This peculiar pattern of activation leads us to hypothesize that resting MCS patients have a bottom-up driven activation of the task positive network and thus are tendentially prone to respond to environmental stimuli, even though in an almost unintentional way