Functional Brain Oscillations: How Oscillations Facilitate Information Representation and Code Memories

The overall aim of the modelling works within this thesis is to lend theoretical evidence to empirical findings from the brain oscillations literature. We therefore hope to solidify and expand the notion that precise spike timing through oscillatory mechanisms facilitates communication, learning, information processing and information representation within the brain. The primary hypothesis of this thesis is that it can be shown computationally that neural de-synchronisations can allow information content to emerge. We do this using two neural network models, the first of which shows how differential rates of neuronal firing can indicate when a single item is being actively represented. The second model expands this notion by creating a complimentary timing mechanism, thus enabling the emergence of qualitive temporal information when a pattern of items is being actively represented. The secondary hypothesis of this thesis is that it can be also be shown computationally that oscillations might play a functional role in learning. Both of the models presented within this thesis propose a sparsely coded and fast learning hippocampal region that engages in the binding of novel episodic information. The first model demonstrates how active cortical representations enable learning to occur in their hippocampal counterparts via a phase-dependent learning rule. The second model expands this notion, creating hierarchical temporal sequences to encode the relative temporal position of cortical representations. We demonstrate in both of these models, how cortical brain oscillations might provide a gating function to the representation of information, whilst complimentary hippocampal oscillations might provide distinct phasic reference points for learning

Neocortical Connectivity during Episodic Memory Formation

During the formation of new episodic memories, a rich array of perceptual information is bound together for long-term storage. However, the brain mechanisms by which sensory representations (such as colors, objects, or individuals) are selected for episodic encoding are currently unknown. We describe a functional magnetic resonance imaging experiment in which participants encoded the association between two classes of visual stimuli that elicit selective responses in the extrastriate visual cortex (faces and houses). Using connectivity analyses, we show that correlation in the hemodynamic signal between face- and place-sensitive voxels and the left dorsolateral prefrontal cortex is a reliable predictor of successful face–house binding. These data support the view that during episodic encoding, “top-down” control signals originating in the prefrontal cortex help determine which perceptual information is fated to be bound into the new episodic memory trace

Phase separation of competing memories along the human hippocampal theta rhythm

Competition between overlapping memories is considered one of the major causes of forgetting, and it is still unknown how the human brain resolves such mnemonic conflict. In the present magnetoencephalography (MEG) study, we empirically tested a computational model that leverages an oscillating inhibition algorithm to minimise overlap between memories. We used a proactive interference task, where a reminder word could be associated with either a single image (non-competitive condition) or two competing images, and participants were asked to always recall the most recently learned word–image association. Time-resolved pattern classifiers were trained to detect the reactivated content of target and competitor memories from MEG sensor patterns, and the timing of these neural reactivations was analysed relative to the phase of the dominant hippocampal 3 Hz theta oscillation. In line with our pre-registered hypotheses, target and competitor reactivations locked to different phases of the hippocampal theta rhythm after several repeated recalls. Participants who behaviourally experienced lower levels of interference also showed larger phase separation between the two overlapping memories. The findings provide evidence that the temporal segregation of memories, orchestrated by slow oscillations, plays a functional role in resolving mnemonic competition by separating and prioritising relevant memories under conditions of high interference

Retrieval induces adaptive forgetting of competing memories via cortical pattern suppression

Remembering a past experience can, surprisingly, cause forgetting. Forgetting arises when other competing traces interfere with retrieval and inhibitory control mechanisms are engaged to suppress the distraction they cause. This form of forgetting is considered to be adaptive because it reduces future interference. The effect of this proposed inhibition process on competing memories has, however, never been observed, as behavioral methods are 'blind' to retrieval dynamics and neuroimaging methods have not isolated retrieval of individual memories. We developed a canonical template tracking method to quantify the activation state of individual target memories and competitors during retrieval. This method revealed that repeatedly retrieving target memories suppressed cortical patterns unique to competitors. Pattern suppression was related to engagement of prefrontal regions that have been implicated in resolving retrieval competition and, critically, predicted later forgetting. Thus, our findings demonstrate a cortical pattern suppression mechanism through which remembering adaptively shapes which aspects of our past remain accessible

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

Cholinergic modulation of cognitive processing: insights drawn from computational models

Acetylcholine plays an important role in cognitive function, as shown by pharmacological manipulations that impact working memory, attention, episodic memory, and spatial memory function. Acetylcholine also shows striking modulatory influences on the cellular physiology of hippocampal and cortical neurons. Modeling of neural circuits provides a framework for understanding how the cognitive functions may arise from the influence of acetylcholine on neural and network dynamics. We review the influences of cholinergic manipulations on behavioral performance in working memory, attention, episodic memory, and spatial memory tasks, the physiological effects of acetylcholine on neural and circuit dynamics, and the computational models that provide insight into the functional relationships between the physiology and behavior. Specifically, we discuss the important role of acetylcholine in governing mechanisms of active maintenance in working memory tasks and in regulating network dynamics important for effective processing of stimuli in attention and episodic memory tasks. We also propose that theta rhythm plays a crucial role as an intermediary between the physiological influences of acetylcholine and behavior in episodic and spatial memory tasks. We conclude with a synthesis of the existing modeling work and highlight future directions that are likely to be rewarding given the existing state of the literature for both empiricists and modelers

An optimal oscillatory phase for pattern reactivation during memory retrieval

Computational models and in vivo studies in rodents suggest that the hippocampal system oscillates between states that are optimal for encoding and states that are optimal for retrieval. Here, we show that in humans, neural signatures of memory reactivation are modulated by the phase of a theta oscillation. Electroencephalography (EEG) was recorded while participants were cued to recall previously learned word-object associations, and time-resolved pattern classifiers were trained to detect neural reactivation of the target objects. Classifier fidelity rhythmically fluctuated at 7 or 8 Hz and was modulated by theta phase across the entire recall period. The phase of optimal classification was shifted approximately 180° between encoding and retrieval. Inspired by animal work, we then computed “classifier-locked averages” to analyze how ongoing theta oscillations behaved around the time points at which the classifier indicated memory retrieval. We found strong theta (7 or 8 Hz) phase consistency approximately 300 ms before the time points of maximal neural memory reactivation. Our findings provide important evidence that the neural signatures of memory retrieval fluctuate and are time locked to the phase of an ongoing theta oscillation

Interaction between theta phase and spike timing-dependent plasticity simulates theta-induced memory effects

Rodent studies suggest that spike timing relative to hippocampal theta activity determines whether potentiation or depression of synapses arise. Such changes also depend on spike timing between presynaptic and postsynaptic neurons, known as spike timing-dependent plasticity (STDP). STDP, together with theta phase-dependent learning, has inspired several computational models of learning and memory. However, evidence to elucidate how these mechanisms directly link to human episodic memory is lacking. In a computational model, we modulate long-term potentiation (LTP) and long-term depression (LTD) of STDP, by opposing phases of a simulated theta rhythm. We fit parameters to a hippocampal cell culture study in which LTP and LTD were observed to occur in opposing phases of a theta rhythm. Further, we modulated two inputs by cosine waves with 0° and asynchronous phase offsets and replicate key findings in human episodic memory. Learning advantage was found for the in-phase condition, compared with the out-of-phase conditions, and was specific to theta-modulated inputs. Importantly, simulations with and without each mechanism suggest that both STDP and theta phase-dependent plasticity are necessary to replicate the findings. Together, the results indicate a role for circuit-level mechanisms, which bridge the gap between slice preparation studies and human memory

Pain-relief learning in flies, rats, and man: basic research and applied perspectives

Memories relating to a painful, negative event are adaptive and can be stored for a lifetime to support preemptive avoidance, escape, or attack behavior. However, under unfavorable circumstances such memories can become overwhelmingly powerful. They may trigger excessively negative psychological states and uncontrollable avoidance of locations, objects, or social interactions. It is therefore obvious that any process to counteract such effects will be of value. In this context, we stress from a basic-research perspective that painful, negative events are "Janus-faced" in the sense that there are actually two aspects about them that are worth remembering: What made them happen and what made them cease. We review published findings from fruit flies, rats, and man showing that both aspects, respectively related to the onset and the offset of the negative event, induce distinct and oppositely valenced memories: Stimuli experienced before an electric shock acquire negative valence as they signal upcoming punishment, whereas stimuli experienced after an electric shock acquire positive valence because of their association with the relieving cessation of pain. We discuss how memories for such punishment-and relief-learning are organized, how this organization fits into the threat-imminence model of defensive behavior, and what perspectives these considerations offer for applied psychology in the context of trauma, panic, and nonsuicidal self-injury