Embedded ensemble encoding hypothesis: The role of the “Prepared” cell

Antic, Srdjan D.; Hines, Michael L.; Lytton, William W.

doi:10.1002/jnr.24240

Cited by 18 publications

(15 citation statements)

References 151 publications

(291 reference statements)

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“…As a consequence, other incoming excitatory postsynaptic potentials (EPSPs), arriving on other dendritic branches, become much more potent drivers of action potential (AP) initiation during the plateau event. The results from the detailed model support a theoretical framework in which plateau potentials allow cortical pyramidal neurons to respond quickly to ongoing network activity and potentially enable synchronized firing to form active neural ensembles (Legenstein and Maass, 2011;Chiovini et al, 2014;Antic et al, 2018).…”

Section: Introductionsupporting

confidence: 58%

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Local glutamate-mediated dendritic plateau potentials change the state of the cortical pyramidal neuron

Gao

Graham

Zhou

et al. 2021

Journal of Neurophysiology

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Dendritic spikes in thin dendritic branches (basal and oblique dendrites) are traditionally inferred from spikelets measured in the cell body. Here, we used laser-spot voltage-sensitive dye imaging in cortical pyramidal neurons (rat brain slices) to investigate the voltage waveforms of dendritic potentials occurring in response to spatially-restricted glutamatergic inputs. Local dendritic potentials lasted 200-500 ms and propagated to the cell body, where they caused sustained 10-20 mV depolarizations. Plateau potentials propagating from dendrite to soma, and action potentials propagating from soma to dendrite, created complex voltage waveforms in the middle of the thin basal dendrite, comprised of local sodium spikelets, local plateau potentials, and back-propagating action potentials, superimposed on each other. Our model replicated these voltage waveforms across a gradient of glutamatergic stimulation intensities. Model then predicted that somatic input resistance (Rin) and membrane time constant (TAU) may reduce during dendritic plateau potential. We then tested these model predictions in real neurons, and found that model correctly predicted the direction of Rin and TAU change, but not the magnitude. In summary, dendritic plateau potentials occurring in basal and oblique branches put pyramidal neurons into an activated neuronal state ("prepared state"), characterized by depolarized membrane potential, and smaller, but faster membrane responses. The prepared state provides a time window of 200-500 ms during which cortical neurons are particularly excitable and capable of following afferent inputs. At the network level, this predicts that sets of cells with simultaneous plateaus would provide cellular substrate for the formation of functional neuronal ensembles.

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Section: Introductionsupporting

confidence: 58%

“…Our model predicts that distally positioned synaptic cluster would produce longer sustained depolarizations compared to the proximally positioned cluster. Therefore, strategic positioning of a distinct group of afferents on the most distal dendritic segments may have an impact on cortical processing of information (Antic et al, 2018).…”

Section: Discussionmentioning

confidence: 99%

Local glutamate-mediated dendritic plateau potentials change the state of the cortical pyramidal neuron

Gao

Graham

Zhou

et al. 2021

Journal of Neurophysiology

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“…15b). Dendritic nonlinearities, such as N-methyl- D -aspartate (NMDA)-mediated plateau potentials evoked by clustered synaptic inputs onto the dendritic tree could also play an important role 47,48 .…”

Section: Discussionmentioning

confidence: 99%

Cortical reliability amid noise and chaos

et al. 2019

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Typical responses of cortical neurons to identical sensory stimuli appear highly variable. It has thus been proposed that the cortex primarily uses a rate code. However, other studies have argued for spike-time coding under certain conditions. The potential role of spike-time coding is directly limited by the internally generated variability of cortical circuits, which remains largely unexplored. Here, we quantify this internally generated variability using a biophysical model of rat neocortical microcircuitry with biologically realistic noise sources. We find that stochastic neurotransmitter release is a critical component of internally generated variability, causing rapidly diverging, chaotic recurrent network dynamics. Surprisingly, the same nonlinear recurrent network dynamics can transiently overcome the chaos in response to weak feed-forward thalamocortical inputs, and support reliable spike times with millisecond precision. Our model shows that the noisy and chaotic network dynamics of recurrent cortical microcircuitry are compatible with stimulus-evoked, millisecond spike-time reliability, resolving a long-standing debate.

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“…Candidate motifs have already been identified in the NMC-model, such as common neighbor motifs 49 and high-dimensional cliques that shape spike correlations between neurons 38 . Dendritic nonlinearities, such as N-Methyl-D-aspartate (NMDA)-mediated plateau potentials evoked by clustered synaptic inputs onto the dendritic tree could also play an important role 50,51 .…”

Section: Discussionmentioning

confidence: 99%

Cortical reliability amid noise and chaos

Nolte

Reimann

King

et al. 2018

Preprint

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Typical responses of cortical neurons to identical sensory stimuli are highly variable. It has thus been proposed that the cortex primarily uses a rate code. However, other studies have argued for spike-time coding under certain conditions. The potential role of spike-time coding is constrained by the intrinsic variability of cortical circuits, which remains largely unexplored. Here, we quantified this intrinsic variability using a biophysical model of rat neocortical microcircuitry with biologically realistic noise sources. We found that stochastic neurotransmitter release is a critical component of this variability, which, amplified by recurrent connectivity, causes rapid chaotic divergence with a time constant on the order of 10-20 milliseconds. Surprisingly, weak thalamocortical stimuli can transiently overcome the chaos, and induce reliable spike times with millisecond precision. We show that this effect relies on recurrent cortical connectivity, and is not a simple effect of feed-forward thalamocortical input. We conclude that recurrent cortical architecture supports millisecond spike-time reliability amid noise and chaotic network dynamics, resolving a long-standing debate.All rights reserved. No reuse allowed without permission.(which was not peer-reviewed) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity.

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Embedded ensemble encoding hypothesis: The role of the “Prepared” cell

Cited by 18 publications

References 151 publications

Local glutamate-mediated dendritic plateau potentials change the state of the cortical pyramidal neuron

Local glutamate-mediated dendritic plateau potentials change the state of the cortical pyramidal neuron

Cortical reliability amid noise and chaos

Cortical reliability amid noise and chaos

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