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Santos-Pata, D.

Publications and source records attributed to Santos-Pata, D..

7 recordsLinked to original sources

Disentangling Mnemonic Metacognition from Confidence by Communication between the Precuneus and Hippocampus

Metacognition, the ability to introspectively monitor ones own performance, remains an area with poorly understood neural mechanisms, particularly regarding the intercommunication among various brain regions. Recent studies have identified the precuneus as a key region in mnemonic metacognitive tasks, while the hippocampus is recognized for its role in memory function. This study aimed to investigate the role of the precuneus and hippocampus in mnemonic metacognition by utilizing intracranial electrode recordings from patients with intractable epilepsy to analyze the correlational dynamics between these regions. Our findings revealed that high gamma activity serve as a key feature in both the precuneus and hippocampus for confidence judgment. Based on signal detection theory (SDT), we discovered that high gamma activity in the precuneus is significantly linked to type 2 sensitivity (meta-d), while hippocampal high gamma activity was primarily linked to type 1 sensitivity (d). Additionally, the correlation between high gamma activity in the hippocampus and precuneus was exclusively related to type 2 sensitivity (meta-d). Temporal analysis indicated that the hippocampus is initially engaged for the memory process, followed by its joint engagement together with the precuneus for confidence generation. These findings elucidate the distinct electrophysiological roles of the hippocampus and precuneus in mnemonic metacognition, providing deeper insights into the neural mechanisms underlying this cognitive process.

neuroscience↗

Sustained hippocampal theta-oscillations reflect experience-dependent learning in bidirectional temporal-order memory retrieval

Navigating within our neighborhood, learning a set of concepts, or memorizing a story, requires remembering the relationship between individual items that are presented sequentially. Theta activity in the mammalian hippocampus has been related to the encoding and recall of relational structures embedding episodic memories. However, how theta oscillations are involved in retrieving temporal order information in opposing directionality (forward vs backward) has not been characterized. Here, using intracranial recordings from 10 human epileptic patients of both genders with hippocampal electrodes, we tested the patients with a temporal order memory task in which they learned the spatial relationship among individual items arranged along a circular track and were tested on both forward-cued and backward-cued retrieval conditions. We found that sustained high-power oscillatory events in the hippocampal theta (2-8 Hz) band, as quantified by Pepisode rate, were higher for the backward conditions during the later stage but not in the earlier stage. The theta Pepisode results are consistent with the behavioral memory performance. In contrast, we observed a stronger effect of forward than backward retrieval for the gamma (30-70 Hz) Pepisode rate irrespective of stages. Our results revealed differential roles of theta vs. gamma oscillations in the retrieval of temporal order and how theta oscillations are specifically implicated in the learning process for efficient retrieval of temporal order memories under opposing directionality. Significance statementWhile the hippocampus is critical to link events into unitary episodes, the effect of repeated experiences, or learning, on these processes is not entirely clear. We discovered that hippocampal theta oscillation in humans is modulated by repeated experiences, which in turn increases the efficacy of backward-cued memory retrieval of temporal order. This study revealed an important physiological signature characterizing the role of experiences and learning in bidirectional temporal memory retrieval. Journal sectionBehavioral/Cognitive

neuroscience↗

Theta coordinates hippocampal-entorhinal ensembles during wake and rest

Precisely timed interactions between hippocampal and cortical neurons during replay epochs are thought to support memory consolidation. Indeed, research has shown replay is associated with heightened hippocampal-cortical synchrony. Yet, many caveats remain in our understanding. Namely, it remains unclear how this offline synchrony comes about, whether it is specific to particular behavioural states and how - if at all - it relates to learning. In this study, we sought to address these questions by analysing coordination between CA1 cells and neurons of the deep layers of the medial entorhinal cortex (dMEC) while rats learned a novel spatial task. During movement, we found a subset of dMEC cell which were particularly locked to hippocampal LFP theta-band oscillations and which were preferentially coordinated with hippocampal replay during offline periods. Further, dMEC synchrony with CA1 replay peaked [~]10ms after replay initiation in CA1, suggesting the distributed replay reflects extra-hippocampal information propagation, and was specific to offline periods. Finally, theta-modulated dMEC cells only became coordinated with replay after an animals first encounter with a novel spatial environment and then showed a striking experience-dependent increase in synchronisation with hippocampal replay trajectories, mirroring the animals acquisition of the novel task and coupling to the hippocampal local field. Together, these findings provide strong support for the hypothesis that synergistic hippocampal-cortical replay supports the consolidation of new memories and highlights phase locking to hippocampal theta oscillations as a potential mechanism by which such cross-structural synchrony comes about. Importantly, as CA1 phase-locking to theta is implicated in the generation of theta sequences, thought to be required for replay expression, we speculate the dMEC theta phase-locking reflects the emergence of distributed hippocampal-dMEC theta sequences and that these may support the commission of memories to long-term cortical storage.

neuroscience↗

Basal forebrain rhythmicity is modulated by the exploration phase of novel environments

Acquaintance to novel environments requires the encoding of spatial memories and the processing of unfamiliar sensory information in the hippocampus. Cholinergic signaling promotes the stabilization of hippocampal long-term potentiation (LTP) and contributes to theta-gamma oscillations balance, which is known to be crucial for learning and memory. However, the oscillatory mechanisms by which cholinergic signals are conveyed to the hippocampus are still poorly defined. We analyzed local field potentials from the basal forebrain (BF), a major source of cholinergic projections to the hippocampus, while rats explored a novel environment, and compared the modulation of BF theta (4-10Hz) and gamma (40-80Hz) frequency bands at distinct stages of spatial exploration. We found that BF theta and gamma display learning stage-related rhythmicity and that theta-gamma coupling is stronger at the later stages of exploration, a phenomenon previously observed in the hippocampus. Overall, our results suggest that the BF-hippocampal cholinergic signaling is conveyed via the stereotypical oscillatory patterns found during mnemonic processes, which questions the origins of the learning-related rhythmic activity found in the hippocampus. KEY-POINTSO_LIBasal forebrain theta oscillations decrease their strength in function of exploration time, as observed in the hippocampus. C_LIO_LIBF gamma ripples (bursting events) are longer after learning. C_LIO_LIBF Theta-gamma coupling increases after initial spatial exploration, suggesting BF cross-frequency coupling relation to the learning stage. C_LI

neuroscience↗

A simplified spiking model of grid-cell scale and intrinsic frequencies

The hexagonal tessellation pattern of grid cells scales up progressively along the dorsal-to-ventral axis of the medial entorhinal cortex (MEC) layer II. This scaling gradient has been hypothesized to originate either from inter population synaptic dynamics as postulated by attractor networks, from projected theta frequencies to different axis levels, as in oscillatory models, or from cellular dynamics dependent on hyperpolarization-activated cation currents. To test the hypothesis that intrinsic cellular properties account for the scale gradient as well as the different oscillatory frequencies observed along the dorsal-to-ventral axis, we have modeled and analyzed data from a population of grid cells simulated with spiking neurons interacting through low-dimensional attractor dynamics. To investigate the causal relationship between oscillatory frequencies and grid scale increase, we analyzed the dominant frequencies of the membrane potential for cells with distinct after-spike dynamics. We observed that intrinsic neuronal membrane properties of simulated cells could induce an increase of grid scale when modulated by after-spike reset values. Differences in the membrane potential oscillatory frequency were observed along the simulated dorsal-to-ventral axis, suggesting that, rather than driving to the increase of grid scale as proposed by interference models of grid cells, they are the result of intrinsic cellular properties of neurons at each axis level. Overall, our results suggest that the after-spike dynamics of cation currents may play a major role in determining the grid cells scale and that oscillatory frequencies are a consequence of intrinsic cellular properties that are specific to different levels of the dorsal-to-ventral axis in the MEC layer II.

neuroscience↗

Human vicarious trial and error is predictive of spatial navigation performance

When learning new environments, rats often pause at decision points and look back and forth over their possible trajectories as if they were imagining the future outcome of their actions, a behavior termed \"Vicarious trial and error\" (VTE). As the animal learns the environmental configuration, rats change from deliberative to habitual behavior, and VTE tends to disappear, suggesting a functional relevance in the early stages of learning. Despite the extensive research on spatial navigation, learning and VTE in the rat model, fewer studies have focused on humans. Here, we tested whether head-scanning behaviors that humans typically exhibit during spatial navigation are as predictive of spatial learning as in the rat. Subjects performed a goal-oriented virtual navigation task in a symmetric environment. Spatial learning was assessed through the analysis of trajectories, timings, and head orientations, under habitual and deliberative spatial navigation conditions. As expected, we found that trajectory length and duration decreased with the trial number, implying that subjects learned the spatial configuration of the environment over trials. Interestingly, IdPhi (a standard metric of VTE) also decreased with the trial number, suggesting that humans benefit from the same head-orientation scanning behavior as rats at spatial decision-points. Moreover, IdPhi captured exclusively at the first decision-point of each trial, was correlated with trial trajectory duration and length. Our findings demonstrate that in VTE is a signature of the stage of spatial learning in humans, and can be used to predict performance in navigation tasks with high accuracy.

animal behavior and cognition↗

Insect behavioral evidence of spatial memories during environmental reconfiguration

Insects are great explorers, able to navigate through long-distance trajectories and successfully find their way back. Their navigational routes cross dynamic environments suggesting adaptation to novel configurations. Arthropods and vertebrates share neural organizational principles and it has been shown that rodents modulate their neural spatial representation accordingly with environmental changes. However, it is unclear whether insects reflexively adapt to environmental changes or retain memory traces of previously explored situations. We sought to disambiguate between insect behavior at environmental novel situations and reconfiguration conditions. An immersive mixed-reality multi-sensory setup was built to replicate multi-sensory cues. We have designed an experimental setup where female crickets Gryllus Bimaculatus were trained to move towards paired auditory and visual cues during primarily phonotactic driven behavior. We hypothesized that insects were capable of identifying sensory modifications in known environments. Our results show that, regardless of the animals history, novel situation conditions did not compromise the animals performance and navigational directionality towards a novel target location. However, in trials where visual and auditory stimuli were spatially decoupled, the animals heading variability towards a previously known location significantly increased. Our findings showed that crickets are able to behaviorally manifest environmental reconfiguration, suggesting the encoding for spatial representation.

animal behavior and cognition↗