Reversed and forward buffering of behavioral spike sequences enables retrospective and prospective retrieval in hippocampal regions CA3 and CA1

Koene, Randal A.; Hasselmo, Michael E.

doi:10.1016/j.neunet.2007.12.029

Cited by 28 publications

(32 citation statements)

References 38 publications

(67 reference statements)

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“…Speculatively, elevated background activity may also play a role in the reactivation of learning-related neural activity during sleep (Ji and Wilson 2007;Louie and Wilson 2001), which promotes memory consolidation. This hypothesis is consistent with a recent computational model, where hippocampal reactivation is driven by persistent input from the entorhinal cortex and dentate gyrus (Koene and Hasselmo 2008). This mechanism, however, does not rule out the possibility of reactivation through intrinsic dynamics.…”

Section: Recalling Temporal Patterns After a Delay Periodsupporting

confidence: 90%

Spiking neurons that keep the rhythm

Thivierge

Cisek

2010

J Comput Neurosci

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Detecting the temporal relationship among events in the environment is a fundamental goal of the brain. Following pulses of rhythmic stimuli, neurons of the retina and cortex produce activity that closely approximates the timing of an omitted pulse. This omitted stimulus response (OSR) is generally interpreted as a transient response to rhythmic input and is thought to form a basis of short-term perceptual memories. Despite its ubiquity across species and experimental protocols, the mechanisms underlying OSRs remain poorly understood. In particular, the highly transient nature of OSRs, typically limited to a single cycle after stimulation, cannot be explained by a simple mechanism that would remain locked to the frequency of stimulation. Here, we describe a set of realistic simulations that capture OSRs over a range of stimulation frequencies matching experimental work. The model does not require an explicit mechanism for learning temporal sequences. Instead, it relies on spike timing-dependent plasticity (STDP), a form of synaptic modification that is sensitive to the timing of pre- and post-synaptic action potentials. In the model, the transient nature of OSRs is attributed to the heterogeneous nature of neural properties and connections, creating intricate forms of activity that are continuously changing over time. Combined with STDP, neural heterogeneity enabled OSRs to complex rhythmic patterns as well as OSRs following a delay period. These results link the response of neurons to rhythmic patterns with the capacity of heterogeneous circuits to produce transient and highly flexible forms of neural activity.

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Section: Recalling Temporal Patterns After a Delay Periodsupporting

confidence: 90%

Spiking neurons that keep the rhythm

Thivierge

Cisek

2010

J Comput Neurosci

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“…Studies aimed at this goal are already beginning to emerge. For instance, a recent theoretical model based on STDP (Koene and Hasselmo, 2008) captures the replay of spatiotemporal sequences of spikes observed in hippocampus during slow-wave sleep (Lee and Wilson, 2002) as well as consummatory behavior (Foster and Wilson, 2006). More generally, the well documented role of STDP in learning temporal sequences (Abbott and Blum, 1996;Bi and Poo, 1999) makes it a promising avenue of exploration toward uncovering the basic mechanisms of learning and memory.…”

Section: Discussionmentioning

confidence: 99%

Nonperiodic Synchronization in Heterogeneous Networks of Spiking Neurons

Thivierge¹,

Cisek²

2008

J. Neurosci.

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Neural synchronization is of wide interest in neuroscience and has been argued to form the substrate for conscious attention to stimuli, movement preparation, and the maintenance of task-relevant representations in active memory. Despite a wealth of possible functions, the mechanisms underlying synchrony are still poorly understood. In particular, in vitro preparations have demonstrated synchronization with no apparent periodicity, which cannot be explained by simple oscillatory mechanisms. Here, we investigate the possible origins of nonperiodic synchronization through biophysical simulations. We show that such aperiodic synchronization arises naturally under a simple set of plausible assumptions, depending crucially on heterogeneous cell properties. In addition, nonperiodicity occurs even in the absence of stochastic fluctuation in membrane potential, suggesting that it may represent an intrinsic property of interconnected networks. Simulations capture some of the key aspects of population-level synchronization in spontaneous network spikes (NSs) and suggest that the intrinsic nonperiodicity of NSs observed in reduced cell preparations is a phenomenon that is highly robust and can be reproduced in simulations that involve a minimal set of realistic assumptions. In addition, a model with spike timing-dependent plasticity can overcome a natural tendency to exhibit nonperiodic behavior. After rhythmic stimulation, the model does not automatically fall back to a state of nonperiodic behavior, but keeps replaying the pattern of evoked NSs for a few cycles. A cluster analysis of synaptic strengths highlights the importance of population-wide interactions in generating this result and describes a possible route for encoding temporal patterns in networks of neurons.

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“…Another line of research asked how multiple stimuli, that are presented sequentially one after another, can be stored as short-term memory without losing the sequence in which the stimuli were presented (Lisman and Idiart, 1995; Jensen and Lisman, 1996; Koene and Hasselmo, 2008). In these models, each memory trace was stored by one neuron that showed persistent firing in a theta frequency (4–14 Hz) due to the CAN current kinetics.…”

Section: Possible Roles Of Can Current In Active Maintenance Of Memormentioning

confidence: 99%

Cholinergic modulation of the CAN current may adjust neural dynamics for active memory maintenance, spatial navigation and time-compressed replay

Yoshida¹,

Knauer²,

Jochems³

2012

Front. Neural Circuits

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Suppression of cholinergic receptors and inactivation of the septum impair short-term memory, and disrupt place cell and grid cell activity in the medial temporal lobe (MTL). Location-dependent hippocampal place cell firing during active waking, when the acetylcholine level is high, switches to time-compressed replay activity during quiet waking and slow-wave-sleep (SWS), when the acetylcholine level is low. However, it remains largely unknown how acetylcholine supports short-term memory, spatial navigation, and the functional switch to replay mode in the MTL. In this paper, we focus on the role of the calcium-activated non-specific cationic (CAN) current which is activated by acetylcholine. The CAN current is known to underlie persistent firing, which could serve as a memory trace in many neurons in the MTL. Here, we review the CAN current and discuss possible roles of the CAN current in short-term memory and spatial navigation. We further propose a novel theoretical model where the CAN current switches the hippocampal place cell activity between real-time and time-compressed sequential activity during encoding and consolidation, respectively.

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Reversed and forward buffering of behavioral spike sequences enables retrospective and prospective retrieval in hippocampal regions CA3 and CA1

Cited by 28 publications

References 38 publications

Spiking neurons that keep the rhythm

Spiking neurons that keep the rhythm

Nonperiodic Synchronization in Heterogeneous Networks of Spiking Neurons

Cholinergic modulation of the CAN current may adjust neural dynamics for active memory maintenance, spatial navigation and time-compressed replay

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