Emergence of physiological oscillation frequencies in a computer model of neocortex

Samuel A. Neymotin, Heekyung Lee, Eunhye Park, Andre Fenton, William W. Lytton

Research output: Contribution to journalArticle

Abstract

Coordination of neocortical oscillations has been hypothesized to underlie the “binding” essential to cognitive function. However, the mechanisms that generate neocortical oscillations in physiological frequency bands remain unknown.We hypothesized that interlaminar relations in neocortex would provide multiple intermediate loops that would play particular roles in generating oscillations, adding different dynamics to the network. We simulated networks from sensory neocortex using nine columns of event-driven rule-based neurons wired according to anatomical data and driven with random white-noise synaptic inputs. We tuned the network to achieve realistic cell firing rates and to avoid population spikes. A physiological frequency spectrum appeared as an emergent property, displaying dominant frequencies that were not present in the inputs or in the intrinsic or activated frequencies of any of the cell groups. We monitored spectral changes while using minimal dynamical perturbation as a methodology through gradual introduction of hubs into individual layers.We found that hubs in layer 2/3 excitatory cells had the greatest influence on overall network activity, suggesting that this subpopulation was a primary generator of theta/beta strength in the network. Similarly, layer 2/3 interneurons appeared largely responsible for gamma activation through preferential attenuation of the rest of the spectrum. The network showed evidence of frequency homeostasis: increased activation of supragranular layers increased firing rates in the network without altering the spectral profile, and alteration in synaptic delays did not significantly shift spectral peaks. Direct comparison of the power spectra with experimentally recorded local field potentials from prefrontal cortex of awake rat showed substantial similarities, including comparable patterns of cross-frequency coupling.

Original languageEnglish (US)
Article number19
JournalFrontiers in Computational Neuroscience
Volume5
DOIs
StatePublished - Apr 19 2011

Fingerprint

Neocortex
Computer Simulation
Interneurons
Prefrontal Cortex
Cognition
Homeostasis
Neurons
Population

Keywords

  • Columns
  • Homeostasis
  • Hubs
  • Neocortex
  • Neuronal-networks
  • Oscillations
  • Simulations
  • Synchrony

ASJC Scopus subject areas

  • Neuroscience (miscellaneous)
  • Cellular and Molecular Neuroscience

Cite this

Emergence of physiological oscillation frequencies in a computer model of neocortex. / Neymotin, Samuel A.; Lee, Heekyung; Park, Eunhye; Fenton, Andre; Lytton, William W.

In: Frontiers in Computational Neuroscience, Vol. 5, 19, 19.04.2011.

Research output: Contribution to journalArticle

Neymotin, Samuel A. ; Lee, Heekyung ; Park, Eunhye ; Fenton, Andre ; Lytton, William W. / Emergence of physiological oscillation frequencies in a computer model of neocortex. In: Frontiers in Computational Neuroscience. 2011 ; Vol. 5.
@article{18d4de92a0b24779bd2f3851bcda18c9,
title = "Emergence of physiological oscillation frequencies in a computer model of neocortex",
abstract = "Coordination of neocortical oscillations has been hypothesized to underlie the “binding” essential to cognitive function. However, the mechanisms that generate neocortical oscillations in physiological frequency bands remain unknown.We hypothesized that interlaminar relations in neocortex would provide multiple intermediate loops that would play particular roles in generating oscillations, adding different dynamics to the network. We simulated networks from sensory neocortex using nine columns of event-driven rule-based neurons wired according to anatomical data and driven with random white-noise synaptic inputs. We tuned the network to achieve realistic cell firing rates and to avoid population spikes. A physiological frequency spectrum appeared as an emergent property, displaying dominant frequencies that were not present in the inputs or in the intrinsic or activated frequencies of any of the cell groups. We monitored spectral changes while using minimal dynamical perturbation as a methodology through gradual introduction of hubs into individual layers.We found that hubs in layer 2/3 excitatory cells had the greatest influence on overall network activity, suggesting that this subpopulation was a primary generator of theta/beta strength in the network. Similarly, layer 2/3 interneurons appeared largely responsible for gamma activation through preferential attenuation of the rest of the spectrum. The network showed evidence of frequency homeostasis: increased activation of supragranular layers increased firing rates in the network without altering the spectral profile, and alteration in synaptic delays did not significantly shift spectral peaks. Direct comparison of the power spectra with experimentally recorded local field potentials from prefrontal cortex of awake rat showed substantial similarities, including comparable patterns of cross-frequency coupling.",
keywords = "Columns, Homeostasis, Hubs, Neocortex, Neuronal-networks, Oscillations, Simulations, Synchrony",
author = "Neymotin, {Samuel A.} and Heekyung Lee and Eunhye Park and Andre Fenton and Lytton, {William W.}",
year = "2011",
month = "4",
day = "19",
doi = "10.3389/fncom.2011.00019",
language = "English (US)",
volume = "5",
journal = "Frontiers in Computational Neuroscience",
issn = "1662-5188",
publisher = "Frontiers Research Foundation",

}

TY - JOUR

T1 - Emergence of physiological oscillation frequencies in a computer model of neocortex

AU - Neymotin, Samuel A.

AU - Lee, Heekyung

AU - Park, Eunhye

AU - Fenton, Andre

AU - Lytton, William W.

PY - 2011/4/19

Y1 - 2011/4/19

N2 - Coordination of neocortical oscillations has been hypothesized to underlie the “binding” essential to cognitive function. However, the mechanisms that generate neocortical oscillations in physiological frequency bands remain unknown.We hypothesized that interlaminar relations in neocortex would provide multiple intermediate loops that would play particular roles in generating oscillations, adding different dynamics to the network. We simulated networks from sensory neocortex using nine columns of event-driven rule-based neurons wired according to anatomical data and driven with random white-noise synaptic inputs. We tuned the network to achieve realistic cell firing rates and to avoid population spikes. A physiological frequency spectrum appeared as an emergent property, displaying dominant frequencies that were not present in the inputs or in the intrinsic or activated frequencies of any of the cell groups. We monitored spectral changes while using minimal dynamical perturbation as a methodology through gradual introduction of hubs into individual layers.We found that hubs in layer 2/3 excitatory cells had the greatest influence on overall network activity, suggesting that this subpopulation was a primary generator of theta/beta strength in the network. Similarly, layer 2/3 interneurons appeared largely responsible for gamma activation through preferential attenuation of the rest of the spectrum. The network showed evidence of frequency homeostasis: increased activation of supragranular layers increased firing rates in the network without altering the spectral profile, and alteration in synaptic delays did not significantly shift spectral peaks. Direct comparison of the power spectra with experimentally recorded local field potentials from prefrontal cortex of awake rat showed substantial similarities, including comparable patterns of cross-frequency coupling.

AB - Coordination of neocortical oscillations has been hypothesized to underlie the “binding” essential to cognitive function. However, the mechanisms that generate neocortical oscillations in physiological frequency bands remain unknown.We hypothesized that interlaminar relations in neocortex would provide multiple intermediate loops that would play particular roles in generating oscillations, adding different dynamics to the network. We simulated networks from sensory neocortex using nine columns of event-driven rule-based neurons wired according to anatomical data and driven with random white-noise synaptic inputs. We tuned the network to achieve realistic cell firing rates and to avoid population spikes. A physiological frequency spectrum appeared as an emergent property, displaying dominant frequencies that were not present in the inputs or in the intrinsic or activated frequencies of any of the cell groups. We monitored spectral changes while using minimal dynamical perturbation as a methodology through gradual introduction of hubs into individual layers.We found that hubs in layer 2/3 excitatory cells had the greatest influence on overall network activity, suggesting that this subpopulation was a primary generator of theta/beta strength in the network. Similarly, layer 2/3 interneurons appeared largely responsible for gamma activation through preferential attenuation of the rest of the spectrum. The network showed evidence of frequency homeostasis: increased activation of supragranular layers increased firing rates in the network without altering the spectral profile, and alteration in synaptic delays did not significantly shift spectral peaks. Direct comparison of the power spectra with experimentally recorded local field potentials from prefrontal cortex of awake rat showed substantial similarities, including comparable patterns of cross-frequency coupling.

KW - Columns

KW - Homeostasis

KW - Hubs

KW - Neocortex

KW - Neuronal-networks

KW - Oscillations

KW - Simulations

KW - Synchrony

UR - http://www.scopus.com/inward/record.url?scp=84937157521&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84937157521&partnerID=8YFLogxK

U2 - 10.3389/fncom.2011.00019

DO - 10.3389/fncom.2011.00019

M3 - Article

VL - 5

JO - Frontiers in Computational Neuroscience

JF - Frontiers in Computational Neuroscience

SN - 1662-5188

M1 - 19

ER -