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Fireflies on the Water How much stochastic is neuronal activity · Synaptic activity is intense and...

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Unité de Neurosciences, Information et Complexité (UNIC) CNRS Gif-sur-Yvette, France http://cns.iaf.cnrs-gif.fr How much stochastic is neuronal activity ? Alain Destexhe FACETS (EU IST) Yayoyi Kusama, Fireflies on the Water Contributors: Theory: Claude Bedard, Sami El Boustani, Olivier Marre, Serafim Rodrigues, Michelle Rudolph (UNIC), Experiments: Diego Contreras (U Penn, USA), Igor Timofeev, Mircea Steriade (Laval University, Canada)
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Page 1: Fireflies on the Water How much stochastic is neuronal activity · Synaptic activity is intense and noisy, essentially Gaussian distributed (both for Vm and conductances) Responsible

Unité de Neurosciences, Information et Complexité (UNIC)

CNRSGif-sur-Yvette, France

http://cns.iaf.cnrs-gif.fr

How much stochastic is neuronal activity ?

Alain Destexhe

FACETS(EU IST)

Yayoyi Kusama, Fireflies on the Water

Contributors:Theory: Claude Bedard, Sami El Boustani, Olivier Marre,

Serafim Rodrigues, Michelle Rudolph (UNIC),Experiments: Diego Contreras (U Penn, USA), Igor Timofeev,

Mircea Steriade (Laval University, Canada)

Page 2: Fireflies on the Water How much stochastic is neuronal activity · Synaptic activity is intense and noisy, essentially Gaussian distributed (both for Vm and conductances) Responsible

WessbergCrist & Nicolelis

(2002)

Ensemble activityin the cortex of abehaving rhesus

monkey

Neuronal activity in awake monkeyComplex spatiotemporal patterns of neuronal discharges

Page 3: Fireflies on the Water How much stochastic is neuronal activity · Synaptic activity is intense and noisy, essentially Gaussian distributed (both for Vm and conductances) Responsible

Plan

1. Characterization of neuronal activity in theneocortex of awake animals

2. Characterization of LFPs

3. Modeling neuronal activity in awake cortex

Page 4: Fireflies on the Water How much stochastic is neuronal activity · Synaptic activity is intense and noisy, essentially Gaussian distributed (both for Vm and conductances) Responsible

Multisite bipolar LFP recordings

Destexhe et al., J. Neurosci.,1999

Awake

Page 5: Fireflies on the Water How much stochastic is neuronal activity · Synaptic activity is intense and noisy, essentially Gaussian distributed (both for Vm and conductances) Responsible

Multisite bipolar LFP recordings

Destexhe et al., J. Neurosci.,1999

Page 6: Fireflies on the Water How much stochastic is neuronal activity · Synaptic activity is intense and noisy, essentially Gaussian distributed (both for Vm and conductances) Responsible

VLC media file(.mp3)

VLC media file(.mp3)Data: Destexhe, Contreras & Steriade, J. Neurosci. 1999

Music: http://www.archive.org/details/NeuronalTones

Multiunit extracellular recordings in awake cats

Wake: Poisson:

Page 7: Fireflies on the Water How much stochastic is neuronal activity · Synaptic activity is intense and noisy, essentially Gaussian distributed (both for Vm and conductances) Responsible

Multiunit extracellular recordings in awake cats

Softky & Koch, J Neurosci. 1993Bedard, Kroger & Destexhe, Phys Rev Lett 2006

Apparent stochastic dynamics!

Page 8: Fireflies on the Water How much stochastic is neuronal activity · Synaptic activity is intense and noisy, essentially Gaussian distributed (both for Vm and conductances) Responsible

Multiunit extracellular recordings in awake cats

Bedard, Kroger & Destexhe, Phys Rev Lett 2006

Apparent stochastic dynamics!

Page 9: Fireflies on the Water How much stochastic is neuronal activity · Synaptic activity is intense and noisy, essentially Gaussian distributed (both for Vm and conductances) Responsible

Multiunit extracellular recordings in awake cats

Marre, El Boustrani, Fregnac & Destexhe(Phys Rev Lett, 2009)

Correlated

Statistics of spike patterns in cat parietal cortex

Uncorrelated

Page 10: Fireflies on the Water How much stochastic is neuronal activity · Synaptic activity is intense and noisy, essentially Gaussian distributed (both for Vm and conductances) Responsible

Intracellular recordings in awake and sleeping animals

(Courtesy of Igor Timofeev, Laval University, Canada)

Page 11: Fireflies on the Water How much stochastic is neuronal activity · Synaptic activity is intense and noisy, essentially Gaussian distributed (both for Vm and conductances) Responsible

Synaptic “noise” in vivo

Pare et al.J Neurophysiol. 1998

Steriade et al.J Neurophysiol. 2001

Destexhe et al.Nature ReviewsNeurosci. 2003

Page 12: Fireflies on the Water How much stochastic is neuronal activity · Synaptic activity is intense and noisy, essentially Gaussian distributed (both for Vm and conductances) Responsible

Conductance measurements in vivo

Paré et al., J. Neurophysiol. 1998Destexhe et al., Nature Reviews Neurosci. 2003

Page 13: Fireflies on the Water How much stochastic is neuronal activity · Synaptic activity is intense and noisy, essentially Gaussian distributed (both for Vm and conductances) Responsible

Characterization of up-states in vivo

Microperfusion of TTX in cat parietal cortexunder ketamine-xylazine anesthesia

Paré et al., J. Neurophysiol. 1998Destexhe et al., Nature Reviews Neurosci. 2003

Page 14: Fireflies on the Water How much stochastic is neuronal activity · Synaptic activity is intense and noisy, essentially Gaussian distributed (both for Vm and conductances) Responsible

Characterization of up-states in vivo

Vm distributionsin different network states

Destexhe & RudolphNeuronal Noise

Rudolph et al.J. Neurophysiol 2005

J. Neurosci. 2007

Page 15: Fireflies on the Water How much stochastic is neuronal activity · Synaptic activity is intense and noisy, essentially Gaussian distributed (both for Vm and conductances) Responsible

Characterization of up-states in vivo

Destexhe & RudolphNeuronal Noise

Rudolph et al.J. Neurophysiol 2005

J. Neurosci. 2007

Conductance measurements in different network states

Page 16: Fireflies on the Water How much stochastic is neuronal activity · Synaptic activity is intense and noisy, essentially Gaussian distributed (both for Vm and conductances) Responsible

Rudolph, Pospischil, Timofeev &Destexhe, J. Neurosci, 2007

Conductance measurementsin awake cats

Extracting conductances from in vivo activity

Page 17: Fireflies on the Water How much stochastic is neuronal activity · Synaptic activity is intense and noisy, essentially Gaussian distributed (both for Vm and conductances) Responsible

Spike-triggered averages of conductances

Rudolph et al.,J. Neurosci,2007

Page 18: Fireflies on the Water How much stochastic is neuronal activity · Synaptic activity is intense and noisy, essentially Gaussian distributed (both for Vm and conductances) Responsible

Characterization of up-states in vitro

Destexhe & RudolphNeuronal Noise

(data fromHasenstaub & McCormick)

Page 19: Fireflies on the Water How much stochastic is neuronal activity · Synaptic activity is intense and noisy, essentially Gaussian distributed (both for Vm and conductances) Responsible

Characterization of up-states in vitro

Destexhe & RudolphNeuronal Noise

(data fromHasenstaub & McCormick)

Page 20: Fireflies on the Water How much stochastic is neuronal activity · Synaptic activity is intense and noisy, essentially Gaussian distributed (both for Vm and conductances) Responsible

Characterization of up-states in vitro

Destexhe & RudolphNeuronal Noise

(data fromHasenstaub & McCormick)

Page 21: Fireflies on the Water How much stochastic is neuronal activity · Synaptic activity is intense and noisy, essentially Gaussian distributed (both for Vm and conductances) Responsible

Synaptic activity is intense and noisy,essentially Gaussian distributed (bothfor Vm and conductances)

Responsible for a “high-conductance state”(3 to 5-fold larger than resting conductance)

Statistics of neuronal activity is very closeto Poisson processes

Importance of inhibition (both for absoluteconductance and for the dynamics ofspike initiation)

Characterizing neuronal activity

Destexhe & Rudolph, Neuronal Noise, Springer 2010

Conclusions

Page 22: Fireflies on the Water How much stochastic is neuronal activity · Synaptic activity is intense and noisy, essentially Gaussian distributed (both for Vm and conductances) Responsible

Plan

1. Characterization of neuronal activity in theneocortex of awake animals

2. Characterization of LFPs

3. Modeling neuronal activity in awake cortex

Page 23: Fireflies on the Water How much stochastic is neuronal activity · Synaptic activity is intense and noisy, essentially Gaussian distributed (both for Vm and conductances) Responsible

PSD of Local Field Potentials

Bedard et al.,Phys Rev Lett 2006

Page 24: Fireflies on the Water How much stochastic is neuronal activity · Synaptic activity is intense and noisy, essentially Gaussian distributed (both for Vm and conductances) Responsible

Modeling LFPs

“Diffusive” LFP Model

Bedard & Destexhe, Biophysical Journal, 2009

Coulomb’s law:

Ionic diffusionin homogeneousmedium

Electrode

PSD of the LFP:

Page 25: Fireflies on the Water How much stochastic is neuronal activity · Synaptic activity is intense and noisy, essentially Gaussian distributed (both for Vm and conductances) Responsible

Modeling LFPs

Bedard & Destexhe, Biophysical Journal, 2009

Page 26: Fireflies on the Water How much stochastic is neuronal activity · Synaptic activity is intense and noisy, essentially Gaussian distributed (both for Vm and conductances) Responsible

Transfer function LFP - Vm activity

Bedard, Rodrigues,Roy, Contreras &DestexheSubmitted

Fitting differenttransferfunctions toexperimentaldata alsosuggestsWarburgimpedance

Page 27: Fireflies on the Water How much stochastic is neuronal activity · Synaptic activity is intense and noisy, essentially Gaussian distributed (both for Vm and conductances) Responsible

“Avalanche dynamics” from LFPs in vivo

Petermann et al., PNAS 2009

Page 28: Fireflies on the Water How much stochastic is neuronal activity · Synaptic activity is intense and noisy, essentially Gaussian distributed (both for Vm and conductances) Responsible

Avalanche analysis from LFP activity (awake cat)

Touboul & Destexhe,PLoS One, 2010

Page 29: Fireflies on the Water How much stochastic is neuronal activity · Synaptic activity is intense and noisy, essentially Gaussian distributed (both for Vm and conductances) Responsible

Avalanche analysis from LFP activity (awake cat)

Page 30: Fireflies on the Water How much stochastic is neuronal activity · Synaptic activity is intense and noisy, essentially Gaussian distributed (both for Vm and conductances) Responsible

Avalanche analysis from LFP activity (awake cat)

Page 31: Fireflies on the Water How much stochastic is neuronal activity · Synaptic activity is intense and noisy, essentially Gaussian distributed (both for Vm and conductances) Responsible

Avalanche analysis from LFP activity (awake cat)

Shuffled LFP peaks (random process!)

Touboul & Destexhe,PLoS One, 2010

Page 32: Fireflies on the Water How much stochastic is neuronal activity · Synaptic activity is intense and noisy, essentially Gaussian distributed (both for Vm and conductances) Responsible

Avalanche analysis from LFP activity (awake cat)

Shuffled LFP peaks (random process!)

Touboul & Destexhe,PLoS One, 2010

Page 33: Fireflies on the Water How much stochastic is neuronal activity · Synaptic activity is intense and noisy, essentially Gaussian distributed (both for Vm and conductances) Responsible

LFPs are broad-band with 1/f scaling at low freq.

1/f scaling can be explained by effect of diffusion

Power-law distributions from LFP peaks can alsobe explained by thresholding procedure

Similar to neuronal activity, a lot can be explainedby purely stochastic mechanisms...

Characterizing LFP activity

Conclusions

Page 34: Fireflies on the Water How much stochastic is neuronal activity · Synaptic activity is intense and noisy, essentially Gaussian distributed (both for Vm and conductances) Responsible

Plan

1. Characterization of neuronal activity in theneocortex of awake animals

2. Characterization of LFPs

3. Modeling neuronal activity in awake cortex

Page 35: Fireflies on the Water How much stochastic is neuronal activity · Synaptic activity is intense and noisy, essentially Gaussian distributed (both for Vm and conductances) Responsible

Network models of self-sustained irregular states

Page 36: Fireflies on the Water How much stochastic is neuronal activity · Synaptic activity is intense and noisy, essentially Gaussian distributed (both for Vm and conductances) Responsible

Network models of asynchronous irregular states

Brunel, J Physiol Paris, 2000

Page 37: Fireflies on the Water How much stochastic is neuronal activity · Synaptic activity is intense and noisy, essentially Gaussian distributed (both for Vm and conductances) Responsible

Self-sustained asynchronous irregular states

Vogels & Abbott,J Neurosci 2005

El Boustani & Destexhe,Neural Computation 2009

Page 38: Fireflies on the Water How much stochastic is neuronal activity · Synaptic activity is intense and noisy, essentially Gaussian distributed (both for Vm and conductances) Responsible

Analysis of AI states

El Boustani et al.,J Physiol Paris, 2007

Page 39: Fireflies on the Water How much stochastic is neuronal activity · Synaptic activity is intense and noisy, essentially Gaussian distributed (both for Vm and conductances) Responsible

Analysis of AI states

El Boustani et al.,J Physiol Paris, 2007

Page 40: Fireflies on the Water How much stochastic is neuronal activity · Synaptic activity is intense and noisy, essentially Gaussian distributed (both for Vm and conductances) Responsible

Analysis of AI states

El Boustani et al.,J Physiol Paris, 2007

Page 41: Fireflies on the Water How much stochastic is neuronal activity · Synaptic activity is intense and noisy, essentially Gaussian distributed (both for Vm and conductances) Responsible

Analysis of AI states

El Boustani et al.,J Physiol Paris, 2007

20 timestoo many!

Page 42: Fireflies on the Water How much stochastic is neuronal activity · Synaptic activity is intense and noisy, essentially Gaussian distributed (both for Vm and conductances) Responsible

Modulation of information transfer by network activity

How to obtain models consistentwith conductance measurements ?

Page 43: Fireflies on the Water How much stochastic is neuronal activity · Synaptic activity is intense and noisy, essentially Gaussian distributed (both for Vm and conductances) Responsible

El Boustani & Destexhe,Neural Computation 2009

Mean-field model of AI statesMacroscopic modeling of AI states in spiking networks

Optical imaging 1 pixel = network ofrandomly-connected neurons

Page 44: Fireflies on the Water How much stochastic is neuronal activity · Synaptic activity is intense and noisy, essentially Gaussian distributed (both for Vm and conductances) Responsible

Mean-field model of AI states

Page 45: Fireflies on the Water How much stochastic is neuronal activity · Synaptic activity is intense and noisy, essentially Gaussian distributed (both for Vm and conductances) Responsible

Mean-field model of AI states

Model predictionNumerical simulation Difference

Page 46: Fireflies on the Water How much stochastic is neuronal activity · Synaptic activity is intense and noisy, essentially Gaussian distributed (both for Vm and conductances) Responsible

Conductancemaps

Mean-field model of AI states

Page 47: Fireflies on the Water How much stochastic is neuronal activity · Synaptic activity is intense and noisy, essentially Gaussian distributed (both for Vm and conductances) Responsible

Network models with realistic conductance patternsBest model: N=16000, 320 synapses/neuron

Vogels & Abbott, J Neurosci, 2005

Page 48: Fireflies on the Water How much stochastic is neuronal activity · Synaptic activity is intense and noisy, essentially Gaussian distributed (both for Vm and conductances) Responsible

Comparison

Network models with realistic conductance patterns

Page 49: Fireflies on the Water How much stochastic is neuronal activity · Synaptic activity is intense and noisy, essentially Gaussian distributed (both for Vm and conductances) Responsible

Conclusions

Randomly connected networks of IF neuronscan generate dynamics which reproduceexperimental observations in the awake brain...

... except for conductances measurements!

Mean-field models can be used to identifynetwork configurations with correctconductance state (work in progress...)

Modeling the awake neocortex

Page 50: Fireflies on the Water How much stochastic is neuronal activity · Synaptic activity is intense and noisy, essentially Gaussian distributed (both for Vm and conductances) Responsible

Thanks to the team...Michelle Rudolph

MartinPospischilSami

El BoustaniClaudeBedard

OlivierMarre

JonathanTouboul

SerafimRodrigues

Page 51: Fireflies on the Water How much stochastic is neuronal activity · Synaptic activity is intense and noisy, essentially Gaussian distributed (both for Vm and conductances) Responsible
Page 52: Fireflies on the Water How much stochastic is neuronal activity · Synaptic activity is intense and noisy, essentially Gaussian distributed (both for Vm and conductances) Responsible

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