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Travelling spindles create necessary conditions for spike-timing-dependent plasticity in humans.

ABSTRACT: Sleep spindles facilitate memory consolidation in the cortex during mammalian non-rapid eye movement sleep. In rodents, phase-locked firing during spindles may facilitate spike-timing-dependent plasticity by grouping pre-then-post-synaptic cell firing within ~25?ms. Currently, microphysiological evidence in humans for conditions conducive for spike-timing-dependent plasticity during spindles is absent. Here, we analyze field potentials and unit firing from middle/upper layers during spindles from 10?×?10 microelectrode arrays at 400??m pitch in humans. We report strong tonic and phase-locked increases in firing and co-firing within 25?ms during spindles, especially those co-occurring with down-to-upstate transitions. Co-firing, spindle co-occurrence, and spindle coherence are greatest within ~2?mm, and high co-firing of units on different contacts depends on high spindle coherence between those contacts. Spindles propagate at ~0.28?m/s in distinct patterns, with correlated cell co-firing sequences. Spindles hence organize spatiotemporal patterns of neuronal co-firing in ways that may provide pre-conditions for plasticity during non-rapid eye movement sleep.

SUBMITTER: Dickey CW

PROVIDER: S-EPMC7884835 | biostudies-literature | 2021 Feb

REPOSITORIES: biostudies-literature

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Travelling spindles create necessary conditions for spike-timing-dependent plasticity in humans.

Dickey Charles W CW Sargsyan Anna A Madsen Joseph R JR Eskandar Emad N EN Cash Sydney S SS Halgren Eric E

Nature communications 20210215 1

Sleep spindles facilitate memory consolidation in the cortex during mammalian non-rapid eye movement sleep. In rodents, phase-locked firing during spindles may facilitate spike-timing-dependent plasticity by grouping pre-then-post-synaptic cell firing within ~25 ms. Currently, microphysiological evidence in humans for conditions conducive for spike-timing-dependent plasticity during spindles is absent. Here, we analyze field potentials and unit firing from middle/upper layers during spindles fro ...[more]

PMID: 33589639

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Project description:Rhythmic activity has been associated with a wide range of cognitive processes including the encoding of sensory information, navigation, the transfer of information and others. Rhythmic activity in the brain has also been suggested to be used for multiplexing information. Multiplexing is the ability to transmit more than one signal via the same channel. Here we focus on frequency division multiplexing, in which different signals are transmitted in different frequency bands. Recent work showed that spike-timing-dependent plasticity (STDP) can facilitate the transfer of rhythmic activity downstream the information processing pathway. However, STDP has also been known to generate strong winner-take-all like competition between subgroups of correlated synaptic inputs. This competition between different rhythmicity channels, induced by STDP, may prevent the multiplexing of information. Thus, raising doubts whether STDP is consistent with the idea of multiplexing. This study explores whether STDP can facilitate the multiplexing of information across multiple frequency channels, and if so, under what conditions. We address this question in a modelling study, investigating the STDP dynamics of two populations synapsing downstream onto the same neuron in a feed-forward manner. Each population was assumed to exhibit rhythmic activity, albeit in a different frequency band. Our theory reveals that the winner-take-all like competitions between the two populations is limited, in the sense that different rhythmic populations will not necessarily fully suppress each other. Furthermore, we found that for a wide range of parameters, the network converged to a solution in which the downstream neuron responded to both rhythms. Yet, the synaptic weights themselves did not converge to a fixed point, rather remained dynamic. These findings imply that STDP can support the multiplexing of rhythmic information, and demonstrate how functionality (multiplexing of information) can be retained in the face of continuous remodeling of all the synaptic weights. The constraints on the types of STDP rules that can support multiplexing provide a natural test for our theory.

Dataset Information

Travelling spindles create necessary conditions for spike-timing-dependent plasticity in humans.

Publications

Travelling spindles create necessary conditions for spike-timing-dependent plasticity in humans.

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