Increased mesiotemporal delta activity characterizes virtual navigation in humans

Hippocampal theta or rhythmic slow activity (RSA) occurring during exploratory behaviors and rapid-eye-movement (REM) sleep is a characteristic and well-identifiable oscillatory rhythm in animals. In contrast, controversy surrounds the existence and electrophysiological correlates of this activity in humans. Some argue that the human hippocampal theta occurs in short and phasic bursts. On the contrary, our earlier studies provide evidence that REM-dependent mesiotemporal RSA is continuous like in animals but instead of the theta it falls in the delta frequency range. Here we used a virtual navigation task in 24 epilepsy patients implanted with foramen ovale electrodes. EEG was analyzed for 1-Hz wide frequency bins up to 10 Hz according to four conditions: resting, non-learning route-following, acquisition and recall. We found progressively increasing spectral power in frequency bins up the 4 Hz across these conditions. No spectral power increase relative to resting was revealed within the traditional theta band and above in any of the navigation conditions. Thus the affected frequency bins were below the theta band and were similar to those characterizing REM sleep in our previous studies providing further indication that it is delta rather than theta that should be regarded as a human analogue of the animal RSA

Working memory load modulates oscillatory activity and the distribution of fast frequencies across frontal theta phase during working memory maintenance

Working memory (WM) is a keystone of our cognitive abilities. Increasing load has been shown to dampen its performance and affect oscillatory neural activity in different frequency bands. Nevertheless, mixed results regarding fast frequencies activity and a lack of research on WM load modulations of cross-frequency phase-amplitude coupling mechanisms preclude a better understanding of the impact of increased WM load levels on brain activity as well as inter-regional communication and coordination supporting WM processes. Hence, we analyzed the EEG activity of 25 participants while performing a delayed-matching-to-sample (DMS) WM task with three WM load levels. Current density power and distribution at the source level for theta, beta, and gamma frequencies during the task's delay period were compared for each pair of WM load conditions. Results showed maximal increases of theta activity in frontal areas and of fast frequencies' activity in posterior regions with WM load, showing the involvement of frontal theta activity in WM maintenance and the control of attentional resources and visual processing by beta and gamma activity. To study whether WM load modulates communication between cortical areas, posterior beta and gamma amplitudes distribution across frontal theta phase was also analysed for those areas showing the largest significant WM load modulations. Higher beta activity amplitude at bilateral cuneus and right middle occipital gyrus, and higher gamma activity amplitude at bilateral posterior cingulate were observed during frontal theta phase peak in low than high memory load conditions. Moreover, greater fast beta amplitude at the right postcentral gyrus was observed during theta phase trough at right middle frontal gyrus in high than low memory load conditions. These results show that WM load modulates whether interregional communication occurs during theoretically optimal or non-optimal time windows, depending on the demands of frontal control of posterior areas required to perform the task successfullyThis study was supported by grants from the Spanish Government, Ministerio de Economía y Competitividad (PSI2014-55316-C3-3-R; PSI2017-89389-C2-2-R), with FEDER Funds; the Galician Government, Consellería de Cultura, Educación e Ordenación Universitaria, Axudas para a Consolidación e Estruturación de Unidades de Investigación Competitivas do Sistema Universitario de Galicia: GRC (GI-1807-USC); Ref: ED431-2017/27, with FEDER funds. D. P. was also supported by the Portuguese Foundation for Science and Technology (FCT) through the fellowship SFRH/BPD/120111/2016S

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

The spectro-contextual encoding and retrieval theory of episodic memory.

The spectral fingerprint hypothesis, which posits that different frequencies of oscillations underlie different cognitive operations, provides one account for how interactions between brain regions support perceptual and attentive processes (Siegel etal., 2012). Here, we explore and extend this idea to the domain of human episodic memory encoding and retrieval. Incorporating findings from the synaptic to cognitive levels of organization, we argue that spectrally precise cross-frequency coupling and phase-synchronization promote the formation of hippocampal-neocortical cell assemblies that form the basis for episodic memory. We suggest that both cell assembly firing patterns as well as the global pattern of brain oscillatory activity within hippocampal-neocortical networks represents the contents of a particular memory. Drawing upon the ideas of context reinstatement and multiple trace theory, we argue that memory retrieval is driven by internal and/or external factors which recreate these frequency-specific oscillatory patterns which occur during episodic encoding. These ideas are synthesized into a novel model of episodic memory (the spectro-contextual encoding and retrieval theory, or "SCERT") that provides several testable predictions for future research

The functional role of dreaming in emotional processes

Dream experience (DE) represents a fascinating condition linked to emotional processes and the human inner world. Although the overlap between REM sleep and dreaming has been overcome, several studies point out that emotional and perceptually vivid contents are more frequent when reported upon awakenings from this sleep stage. Actually, it is well-known that REM sleep plays a pivotal role in the processing of salient and emotional waking-life experiences, strongly contributing to the emotional memory consolidation. In this vein, we highlighted that, to some extent, neuroimaging studies showed that the processes that regulate dreaming and emotional salience in sleep mentation share similar neural substrates of those controlling emotions during wakefulness. Furthermore, the research on EEG correlates of the presence/absence of DE and the results on EEG pattern related to the incorporated memories converged to assign a crucial role of REM theta oscillations in emotional re-processing. In particular, the theta activity is involved in memory processes during REM sleep as well as during the waking state, in line with the continuity hypothesis. Also, the gamma activity seems to be related to emotional processes and dream recall as well as to lucid dreams. Interestingly, similar EEG correlates of DE have been found in clinical samples when nightmares or dreams occur. Research on clinical samples revealed that promoting the rehearsal of frightening contents aimed to change them is a promising method to treat nightmares, and that lucid dreams are associated with an attenuation of nightmares. In this view, DE can defuse emotional traumatic memories when the emotional regulation and the fear extinction mechanisms are compromised by traumatic and frightening events. Finally, dreams could represent a sort of simulation of reality, providing the possibility to create a new scenario with emotional mastery elements to cope with dysphoric items included in nightmares. In addition, it could be hypothesized that the insertion of bizarre items besides traumatic memories might be functional to “impoverish” the negative charge of the experiences

Improving episodic memory: frontal-midline theta neurofeedback training increases source memory performance

Cognitive and neurofeedback training (NFT) studies have demonstrated that training-induced alterations of frontal-midline (FM) theta activity (4-8 Hz) transfer to cognitive control processes. Given that FM theta oscillations are assumed to provide top-down control for episodic memory retrieval, especially for source retrieval, that is, accurate recollection of contextual details of prior episodes, the present study investigated whether FM theta NFT transfers to memory control processes. It was assessed (1) whether FM theta NFT improves source retrieval and modulates its underlying EEG characteristics and (2) whether this transfer extends over two posttests. Over seven NFT sessions, thetraining group who trained individual FM theta activity showed greater FM theta increase than an active control group who trained randomly chosen frequency bands. The training group showed better source retrieval in a posttraining session performed 13 days after NFT and their performance increasesfrom pre- to both posttraining sessions were predicted by NFT theta increases. Thus, training-induced enhancement of memory control processes seems to protect newly formed memories from proactive interference of previously learned information. EEG analyses revealed that during pretest both groups showed source memory specific theta activity at frontal and parietal sites. Surprisingly, training-induced improvements in source retrieval tended to be accompanied by less prestimulus FM theta activity, which was predicted by NFT theta change for the training but not the control group, suggesting a more efficient use of memory control processes after training. The present findings provide unique evidence for the enhancement of memory control processes by FM theta NFT

Lingering Sound: Event-Related Phase-Amplitude Coupling and Phase-Locking in Fronto-Temporo-Parietal Functional Networks During Memory Retrieval of Music Melodies

Brain oscillations and connectivity have emerged as promising measures of evaluating memory processes, including encoding, maintenance, and retrieval, as well as the related executive function. Although many studies have addressed the neural mechanisms underlying working memory, most of these studies have focused on the visual modality. Neurodynamics and functional connectivity related to auditory working memory are yet to be established. In this study, we explored the dynamic of high density (128-channel) electroencephalography (EEG) in a musical delayed match-to-sample task (DMST), in which 36 participants were recruited and were instructed to recognize and distinguish the target melodies from similar distractors. Event-related spectral perturbations (ERSPs), event-related phase-amplitude couplings (ERPACs), and phase-locking values (PLVs) were used to determine the corresponding brain oscillations and connectivity. First, we observed that low-frequency oscillations in the frontal, temporal, and parietal regions were increased during the processing of both target and distracting melodies. Second, the cross-frequency coupling between low-frequency phases and high-frequency amplitudes was elevated in the frontal and parietal regions when the participants were distinguishing between the target from distractor, suggesting that the phase-amplitude coupling could be an indicator of neural mechanisms underlying memory retrieval. Finally, phase-locking, an index evaluating brain functional connectivity, revealed that there was fronto-temporal phase-locking in the theta band and fronto-parietal phase-locking in the alpha band during the recognition of the two stimuli. These findings suggest the existence of functional connectivity and the phase-amplitude coupling in the neocortex during musical memory retrieval, and provide a highly resolved timeline to evaluate brain dynamics. Furthermore, the inter-regional phase-locking and phase-amplitude coupling among the frontal, temporal and parietal regions occurred at the very beginning of musical memory retrieval, which might reflect the precise timing when cognitive resources were involved in the retrieval of targets and the rejection of similar distractors. To the best of our knowledge, this is the first EEG study employing a naturalistic task to study auditory memory processes and functional connectivity during memory retrieval, results of which can shed light on the use of natural stimuli in studies that are closer to the real-life applications of cognitive evaluations, mental treatments, and brain-computer interface

Post-training load-related changes of auditory working memory: An EEG study

Working memory (WM) refers to the temporary retention and manipulation of information, and its capacity is highly susceptible to training. Yet, the neural mechanisms that allow for increased performance under demanding conditions are not fully understood. We expected that post-training efficiency in WM performance modulates neural processing during high load tasks. We tested this hypothesis, using electroencephalography (EEG) (N = 39), by comparing source space spectral power of healthy adults performing low and high load auditory WM tasks. Prior to the assessment, participants either underwent a modality-specific auditory WM training, or a modality-irrelevant tactile WM training, or were not trained (active control). After a modality-specific training participants showed higher behavioral performance, compared to the control. EEG data analysis revealed general effects of WM load, across all training groups, in the theta-, alpha-, and beta-frequency bands. With increased load theta-band power increased over frontal, and decreased over parietal areas. Centro-parietal alpha-band power and central beta-band power decreased with load. Interestingly, in the high load condition a tendency toward reduced beta-band power in the right medial temporal lobe was observed in the modality-specific WM training group compared to the modality-irrelevant and active control groups. Our finding that WM processing during the high load condition changed after modality-specific WM training, showing reduced beta-band activity in voice-selective regions, possibly indicates a more efficient maintenance of task-relevant stimuli. The general load effects suggest that WM performance at high load demands involves complementary mechanisms, combining a strengthening of task-relevant and a suppression of task-irrelevant processing