Propagating Neural Source Revealed by Doppler Shift of Population Spiking Frequency

Zhang, Mingming; Shivacharan, Rajat S.; Chiang, Chia Chu; Gonzalez‐Reyes, Luis E.; Durand, Dominique M.

doi:10.1523/jneurosci.3525-15.2016

Cited by 11 publications

(33 citation statements)

References 45 publications

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“…Based on the structure of the longitudinal hippocampal slice, ephaptic coupling-mediated activity should be able to propagate in both directions when the activity initiates in the middle of the cell layer. This feature was observed in the present study (Figs 5B,8B and 10D) and in a previous study (Zhang et al 2016). Observation of the bidirectional propagation is highly dependent on where the activity initiated.…”

Section: Siapassupporting

confidence: 91%

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Slow periodic activity in the longitudinal hippocampal slice can self‐propagate non‐synaptically by a mechanism consistent with ephaptic coupling

Chiang

Shivacharan

Wei

et al. 2018

The Journal of Physiology

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Key points Slow periodic activity can propagate with speeds around 0.1 m s−1 and be modulated by weak electric fields. Slow periodic activity in the longitudinal hippocampal slice can propagate without chemical synaptic transmission or gap junctions, but can generate electric fields which in turn activate neighbouring cells. Applying local extracellular electric fields with amplitude in the range of endogenous fields is sufficient to modulate or block the propagation of this activity both in the in silico and in the in vitro models. Results support the hypothesis that endogenous electric fields, previously thought to be too small to trigger neural activity, play a significant role in the self‐propagation of slow periodic activity in the hippocampus. Experiments indicate that a neural network can give rise to sustained self‐propagating waves by ephaptic coupling, suggesting a novel propagation mechanism for neural activity under normal physiological conditions. Abstract Slow oscillations are a standard feature observed in the cortex and the hippocampus during slow wave sleep. Slow oscillations are characterized by low‐frequency periodic activity (<1 Hz) and are thought to be related to memory consolidation. These waves are assumed to be a reflection of the underlying neural activity, but it is not known if they can, by themselves, be self‐sustained and propagate. Previous studies have shown that slow periodic activity can be reproduced in the in vitro preparation to mimic in vivo slow oscillations. Slow periodic activity can propagate with speeds around 0.1 m s−1 and be modulated by weak electric fields. In the present study, we show that slow periodic activity in the longitudinal hippocampal slice is a self‐regenerating wave which can propagate with and without chemical or electrical synaptic transmission at the same speeds. We also show that applying local extracellular electric fields can modulate or even block the propagation of this wave in both in silico and in vitro models. Our results support the notion that ephaptic coupling plays a significant role in the propagation of the slow hippocampal periodic activity. Moreover, these results indicate that a neural network can give rise to sustained self‐propagating waves by ephaptic coupling, suggesting a novel propagation mechanism for neural activity under normal physiological conditions.

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Section: Siapassupporting

confidence: 91%

“…This feature was observed in the present study (Figs B , B and D ) and in a previous study (Zhang et al . ). Observation of the bidirectional propagation is highly dependent on where the activity initiated.…”

Section: Discussionmentioning

confidence: 99%

Slow periodic activity in the longitudinal hippocampal slice can self‐propagate non‐synaptically by a mechanism consistent with ephaptic coupling

Chiang

Shivacharan

Wei

et al. 2018

The Journal of Physiology

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“…Yet the origin of these waves and their mechanism of propagation are difficult to be determined in-vivo . Similar waves at similar speeds have been observed in-vitro in the hippocampus under epileptic conditions 5 , 6 and the cortex under normal physiological conditions 7 . We have observed fast spontaneous 4-AP-induced inter-ictal spikes propagating at a speed of approximately 0.1 m/s as well as the source of the spike propagating simultaneously at a slower speed of approximately 0.01 m/s.…”

Section: Introductionsupporting

confidence: 79%

“…The existence of a neural source slowly propagating in the hippocampus was previously inferred from a microelectrode array data since it could not be observed electrically 6 . To observe directly this slow moving wave along the cell layer, optical signals from different locations were reconstructed in the time domain and filtered with a 1 Hz low-pass filter (Fig.…”

Section: Resultsmentioning

confidence: 99%

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Slow moving neural source in the epileptic hippocampus can mimic progression of human seizures

Chiang

Wei

Ananthakrishnan

et al. 2018

Sci Rep

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Fast and slow neural waves have been observed to propagate in the human brain during seizures. Yet the nature of these waves is difficult to study in a surgical setting. Here, we report an observation of two different traveling waves propagating in the in-vitro epileptic hippocampus at speeds similar to those in the human brain. A fast traveling spike and a slow moving wave were recorded simultaneously with a genetically encoded voltage sensitive fluorescent protein (VSFP Butterfly 1.2) and a high speed camera. The results of this study indicate that the fast traveling spike is NMDA-sensitive but the slow moving wave is not. Image analysis and model simulation demonstrate that the slow moving wave is moving slowly, generating the fast traveling spike and is, therefore, a moving source of the epileptiform activity. This slow moving wave is associated with a propagating neural calcium wave detected with calcium dye (OGB-1) but is independent of NMDA receptors, not related to ATP release, and much faster than those previously recorded potassium waves. Computer modeling suggests that the slow moving wave can propagate by the ephaptic effect like epileptiform activity. These findings provide an alternative explanation for slow propagation seizure wavefronts associated with fast propagating spikes.

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Doppler Frequency‐Shift Information Processing in WO_x‐Based Memristive Synapse for Auditory Motion Perception

et al. 2023

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Auditory motion perception is one crucial capability to decode and discriminate the spatiotemporal information for neuromorphic auditory systems. Doppler frequency‐shift feature and interaural time difference (ITD) are two fundamental cues of auditory information processing. In this work, the functions of azimuth detection and velocity detection, as the typical auditory motion perception, are demonstrated in a WOx‐based memristive synapse. The WOx memristor presents both the volatile mode (M1) and semi‐nonvolatile mode (M2), which are capable of implementing the high‐pass filtering and processing the spike trains with a relative timing and frequency shift. In particular, the Doppler frequency‐shift information processing for velocity detection is emulated in the WOx memristor based auditory system for the first time, which relies on a scheme of triplet spike‐timing‐dependent‐plasticity in the memristor. These results provide new opportunities for the mimicry of auditory motion perception and enable the auditory sensory system to be applied in future neuromorphic sensing.

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Propagating Neural Source Revealed by Doppler Shift of Population Spiking Frequency

Cited by 11 publications

References 45 publications

Slow periodic activity in the longitudinal hippocampal slice can self‐propagate non‐synaptically by a mechanism consistent with ephaptic coupling

Slow periodic activity in the longitudinal hippocampal slice can self‐propagate non‐synaptically by a mechanism consistent with ephaptic coupling

Slow moving neural source in the epileptic hippocampus can mimic progression of human seizures

Doppler Frequency‐Shift Information Processing in WO_x‐Based Memristive Synapse for Auditory Motion Perception

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Propagating Neural Source Revealed by Doppler Shift of Population Spiking Frequency

Cited by 11 publications

References 45 publications

Slow periodic activity in the longitudinal hippocampal slice can self‐propagate non‐synaptically by a mechanism consistent with ephaptic coupling

Slow periodic activity in the longitudinal hippocampal slice can self‐propagate non‐synaptically by a mechanism consistent with ephaptic coupling

Slow moving neural source in the epileptic hippocampus can mimic progression of human seizures

Doppler Frequency‐Shift Information Processing in WOx‐Based Memristive Synapse for Auditory Motion Perception

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Product

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Doppler Frequency‐Shift Information Processing in WO_x‐Based Memristive Synapse for Auditory Motion Perception