The evolving concept of the intrinsic hippocampal theta gamma oscillator

Cataldi, Mauro

doi:10.2741/s505

Cited by 10 publications

(5 citation statements)

References 74 publications

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“…In our model, “L1” is ordinarily silent and is disinhibited by activity from an external Unit, oscillating with a theta period. Although recent data suggest that a theta rhythm can also be internally generated within hippocampal circuits ( Cataldi and Vigliotti, 2018 ), as done in our previous model, or modulated by other hippocampal structures such as the entorhinal cortex ( Schlesiger et al, 2015 ), a more common idea is that the theta rhythm originates from an external structure: this may be the septum ( Salib et al, 2019 ), or a resonance within the Papez circuit (including the mammillary bodies, the mammillothalamic tract, and the anterior thalamic nuclei; Vertes et al, 2001 ; Dillingham et al, 2021 ). In particular, Salib et al (2019) suggest that the septum can act by disinhibiting the hippocampus with a mechanism analogous to the one included in our model.…”

Section: Discussionmentioning

confidence: 99%

Modeling the contribution of theta-gamma coupling to sequential memory, imagination, and dreaming

Pirazzini,

Ursino

2024

Front. Neural Circuits

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Gamma oscillations nested in a theta rhythm are observed in the hippocampus, where are assumed to play a role in sequential episodic memory, i.e., memorization and retrieval of events that unfold in time. In this work, we present an original neurocomputational model based on neural masses, which simulates the encoding of sequences of events in the hippocampus and subsequent retrieval by exploiting the theta-gamma code. The model is based on a three-layer structure in which individual Units oscillate with a gamma rhythm and code for individual features of an episode. The first layer (working memory in the prefrontal cortex) maintains a cue in memory until a new signal is presented. The second layer (CA3 cells) implements an auto-associative memory, exploiting excitatory and inhibitory plastic synapses to recover an entire episode from a single feature. Units in this layer are disinhibited by a theta rhythm from an external source (septum or Papez circuit). The third layer (CA1 cells) implements a hetero-associative net with the previous layer, able to recover a sequence of episodes from the first one. During an encoding phase, simulating high-acetylcholine levels, the network is trained with Hebbian (synchronizing) and anti-Hebbian (desynchronizing) rules. During retrieval (low-acetylcholine), the network can correctly recover sequences from an initial cue using gamma oscillations nested inside the theta rhythm. Moreover, in high noise, the network isolated from the environment simulates a mind-wandering condition, randomly replicating previous sequences. Interestingly, in a state simulating sleep, with increased noise and reduced synapses, the network can “dream” by creatively combining sequences, exploiting features shared by different episodes. Finally, an irrational behavior (erroneous superimposition of features in various episodes, like “delusion”) occurs after pathological-like reduction in fast inhibitory synapses. The model can represent a straightforward and innovative tool to help mechanistically understand the theta-gamma code in different mental states.

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Section: Discussionmentioning

confidence: 99%

Modeling the contribution of theta-gamma coupling to sequential memory, imagination, and dreaming

Pirazzini,

Ursino

2024

Front. Neural Circuits

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“…Different brain regions are involved in generation of the gamma rhythm (Whittington et al., 2011 ). In fact, all mechanisms responsible for the components of EEG spectra and their functional interrelations are still poorly understood (Cataldi & Vigliotti, 2018 ; Jing et al., 2016 ).…”

Section: Discussionmentioning

confidence: 99%

Structural changes in the neocortex as correlates of variations in EEG spectra and seizure susceptibility in rat brains with different degrees of dysplasia

Setkowicz

Gzieło

Kielbinski

et al. 2021

J of Comparative Neurology

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Disturbances of the early stages of neurogenesis lead to irreversible changes in the structure of the mature brain and its functional impairment, including increased excitability, which may be the basis for drug‐resistant epilepsy. The range of possible clinical symptoms is as wide as the different stages of disturbed neurogenesis may be. In this study, we used a quadruple model of brain dysplasia by comparing structural and functional disorders in animals whose neurogenesis was disturbed with a single dose of 1 Gy of gamma rays at one of the four stages of neurogenesis, that is, on days 13, 15, 17, or 19 of prenatal development. When reached adulthood, the prenatally irradiated rats received EEG teletransmitter implantation. Thereafter, pilocarpine was administered and significant differences in susceptibility to seizure behavioral symptoms were detected depending on the degree of brain dysplasia. Before, during, and after the seizures significant correlations were found between the density of parvalbumin‐immunopositive neurons located in the cerebral cortex and the intensity of behavioral seizure symptoms or increases in the power of particular EEG bands. Neurons expressing calretinin or NPY showed also dysplasia‐related increases without, however, correlations with parameters of seizure intensity. The results point to significant roles of parvalbumin‐expressing interneurons, and also to expression of NPY—an endogenous anticonvulsant and neuroprotectant reducing susceptibility to seizures and supporting neuronal survival.

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“…A more traditional hypothesis is that the theta rhythm is generated in the septum, which possibly acts as a pacemaker for theta activity (Pignatelli et al 2012) and from there is transmitted to hippocampal neurons (Roux and Uhlhaas 2014). However, more recent data have shown that oscillations in the theta range can be recorded in hippocampal preparations in vitro, thus confirming that the hippocampus itself can act as a theta oscillator (Cataldi and Vigliotti 2018).…”

Section: Basic Model Assumptions and Layersmentioning

confidence: 99%

A model of working memory for encoding multiple items and ordered sequences exploiting the theta-gamma code

2022

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Recent experimental evidence suggests that oscillatory activity plays a pivotal role in the maintenance of information in working memory, both in rodents and humans. In particular, cross-frequency coupling between theta and gamma oscillations has been suggested as a core mechanism for multi-item memory. The aim of this work is to present an original neural network model, based on oscillating neural masses, to investigate mechanisms at the basis of working memory in different conditions. We show that this model, with different synapse values, can be used to address different problems, such as the reconstruction of an item from partial information, the maintenance of multiple items simultaneously in memory, without any sequential order, and the reconstruction of an ordered sequence starting from an initial cue. The model consists of four interconnected layers; synapses are trained using Hebbian and anti-Hebbian mechanisms, in order to synchronize features in the same items, and desynchronize features in different items. Simulations show that the trained network is able to desynchronize up to nine items without a fixed order using the gamma rhythm. Moreover, the network can replicate a sequence of items using a gamma rhythm nested inside a theta rhythm. The reduction in some parameters, mainly concerning the strength of GABAergic synapses, induce memory alterations which mimic neurological deficits. Finally, the network, isolated from the external environment (“imagination phase”) and stimulated with high uniform noise, can randomly recover sequences previously learned, and link them together by exploiting the similarity among items.

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The evolving concept of the intrinsic hippocampal theta gamma oscillator

Cited by 10 publications

References 74 publications

Modeling the contribution of theta-gamma coupling to sequential memory, imagination, and dreaming

Modeling the contribution of theta-gamma coupling to sequential memory, imagination, and dreaming

Structural changes in the neocortex as correlates of variations in EEG spectra and seizure susceptibility in rat brains with different degrees of dysplasia

A model of working memory for encoding multiple items and ordered sequences exploiting the theta-gamma code

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