Functional
consequences of correlated excitatory and inhibitory conductances in
cortical networks
Jens Kremkow1, 2, 3 ,
Laurent U. Perrinet1, Guillaume S. Masson1
and Ad Aertsen2, 3
(1) |
Institut de Neurosciences
Cognitives de la Méditerranée, UMR6193 CNRS—Aix-Marseille Université, 31
chemin Joseph Aiguier, 13402 Marseille Cedex 20, France |
(2) |
Neurobiology and
Biophysics, Faculty of Biology, Albert-Ludwig University,
Schänzlestrasse 1, 79104 Freiburg, Germany |
(3) |
Bernstein Center for
Computational Neuroscience, Hansastrasse 9A, 79104 Freiburg,
Germany |
Received: 19 March 2009 Revised:
8 April 2010 Accepted: 20 April 2010 Published
online: 19 May 2010
Action Editor: X.-J. Wang
Abstract Neurons
in the neocortex receive a large number of excitatory and inhibitory
synaptic inputs. Excitation and inhibition dynamically
balance each other, with inhibition lagging excitation by
only few milliseconds. To characterize the functional consequences
of such correlated excitation and inhibition, we studied
models in which this correlation structure is induced by feedforward
inhibition (FFI). Simple circuits show that an effective FFI
changes the integrative behavior of neurons such that only synchronous
inputs can elicit spikes, causing the responses to be sparse
and precise. Further, effective FFI increases the selectivity
for propagation of synchrony through a feedforward network,
thereby increasing the stability to background activity. Last,
we show that recurrent random networks with effective
inhibition are more likely to exhibit dynamical network activity states
as have been observed in vivo. Thus, when a
feedforward signal path is embedded in such recurrent network, the
stabilizing effect of effective inhibition
creates an suitable substrate for signal propagation. In
conclusion, correlated excitation and inhibition support the notion
that synchronous spiking may be important for cortical
processing.
Keywords Correlated
conductances - Synaptic integration - Sparse
coding - Signal propagation
References
Abeles, M. (1991). Corticonics:
Neural circuits of the cerebral cortex. Cambridge University Press.
|
|
Abeles, M., Hayon, G., &
Lehmann, D. (2004). Modeling compositionality by dynamic binding of
synfire chains. Journal of Computational Neuroscience, 17(2),
179–201.
|
|
Aertsen, A., Diesmann, M., &
Gewaltig, M.-O. (1996). Propagation of synchronous spiking activity in
feedforward neural networks.
Journal of Physiology (Paris), 90(3–4),
243–247.
|
|
Assisi, C. G., Stopfer, M.,
Laurent, G., & Bazhenov, M. (2007). Adaptive regulation of
sparseness by feedforward inhibition.
Nature Neuroscience, 10(9), 1176–1184.
|
|
Atallah, B. V., & Scanziani, M.
(2009). Instantaneous modulation of gamma oscillation frequency by
balancing excitation with
inhibition. Neuron, 62(4), 566–577.
|
|
Aviel, Y., Mehring, C., Abeles, M.,
& Horn, D. (2003). On embedding synfire chains in a balanced
network. Neural Computation, 15(6), 1321–1340.
|
|
Brémaud, A., West, D. C., &
Thomson, A. M. (2007). Binomial parameters differ across neocortical
layers and with different
classes of connections in adult rat and cat neocortex.
Proceedings of the National Academy of Sciences of the United States
of America, 104(35), 14134–14139.
|
|
Braitenberg, V., & Schüz, A.
(1991). Cortex: Anatomy of the cortex: Statistics and geometry.
Springer.
|
|
Brunel, N. (2000). Dynamics of
sparsely connected networks of excitatory and inhibitory spiking
neurons. Journal of Computational Neuroscience, 8(3), 183–208.
|
|
Bruno, R. M., & Sakmann, B.
(2006). Cortex is driven by weak but synchronously active
thalamocortical synapses. Science, 312(5780), 1622–1627.
|
|
Buzsáki, G. (1984). Feed-forward
inhibition in the hippocampal formation. Progress in Neurobiology, 22(2),
131–153.
|
|
Cruikshank, S. J., Lewis, T. J.,
& Connors, B. W. (2007). Synaptic basis for intense thalamocortical
activation of feedforward
inhibitory cells in neocortex. Nature Neuroscience,
10(4), 462–468.
|
|
Davison, A. P., Brüderle, D.,
Eppler, J. M., Kremkow, J., Muller, E., Pecevski, D., et al. (2009).
PyNN: A common interface
for neuronal network simulators. Frontiers in
Neuroinformatics, 2, 11. doi:10.3389/neuro.11/011.2008.
|
|
Delorme, A. (2003). Early cortical
orientation selectivity: How fast inhibition decodes the order of spike
latencies. Journal of Computational Neuroscience, 15(3),
357–365.
|
|
Destexhe, A., Contreras, D., &
Steriade, M. (1998). Mechanisms underlying the synchronizing action of
corticothalamic feedback
through inhibition of thalamic relay cells. Journal
of Neurophysiology, 79(2), 999–1016.
|
|
Destexhe, A., Rudolph, M., &
Paré, D. (2003). The high-conductance state of neocortical neurons in
vivo. Nature Reviews. Neuroscience, 4(9), 739–751.
|
|
Diesmann, M., Gewaltig, M.-O.,
& Aertsen, A. (1999). Stable propagation of synchronous spiking in
cortical neural networks.
Nature, 402(6761), 529–533.
|
|
Eppler, J. M., Helias, M., Muller,
E., Diesmann, M., & Gewaltig, M.-O. (2009). PyNEST: A convenient
interface to the nest
simulator. Frontiers in Neuroinformatics, 2,
12. doi:10.3389/neuro.11/012.2008
|
|
Gerstein, G., & Mandelbrot, B.
(1964). Random walk Models for the spike activity of a single neuron. Biophysical
Journal, 4, 41–68.
|
|
Gewaltig, M.-O., & Diesmann,
M. (2007). NEST (neural simulation tool). Scholarpedia, 2(4),
1430.
|
|
Gewaltig, M.-O., Diesmann, M.,
& Aertsen, A. (2001). Propagation of cortical synfire activity:
Survival probability in single
trials and stability in the mean. Neural Networks,
14(6–7), 657–673.
|
|
Gibson, J. R., Beierlein, M.,
& Connors, B. W. (1999). Two networks of electrically coupled
inhibitory neurons in neocortex.
Nature, 402(6757), 75–79.
|
|
Haider, B., Krause,M. R.,
Duque,A., Yu, Y., Touryan, J., Mazer, J. A., et al. (2010). Synaptic and
network mechanisms of sparse
and reliable visual cortical activity during
nonclassical receptive field stimulation. Neuron, 65(1), 107–121.
|
|
Hasenstaub, A. R., Shu, Y.,
Haider, B., Kraushaar, U., Duque, A., & McCormick, D. (2005).
Inhibitory postsynaptic potentials
carry synchronized frequency information in active
cortical networks. Neuron, 47(3), 423–435.
|
|
Higley, M. J., & Contreras, D.
(2006). Balanced excitation and inhibition determine spike timing
during frequency adaptation.
Journal of Neuroscience, 26(2), 448–457.
|
|
Hirsch, J. A., & Gilbert, C.
D. (1991). Synaptic physiology of horizontal connections in the cat’s
visual cortex. Journal of Neuroscience, 11(6), 1800–1809.
|
|
Hellwig, B. (2000). A quantitative
analysis of the local connectivity between pyramidal neurons in layers
2/3 of the rat visual
cortex. Biological Cybernetics, 82(2), 111–121.
|
|
Inoue, T., & Imoto, K. (2006).
Feedforward inhibitory connections from multiple thalamic cells to
multiple regular-spiking
cells in layer 4 of the somatosensory cortex. Journal
of Neurophysiology, 96(4), 1746–1754.
|
|
Kapfer, C., Glickfeld, L. L.,
Atallah, B. V., & Scanziani, M. (2007). Supralinear increase of
recurrent inhibition during
sparse activity in the somatosensory cortex. Nature
Neuroscience, 10(6), 743–753.
|
|
Kremkow, J., Perrinet, L.,
Aertsen, A., Masson, G. S. (2008a). Functional properties of
feed-forward inhibition. Proc NeuroComp
2008
|
|
Kremkow, J., Perrinet, L., Baudot,
P., Levy, M., Marre, O., Monier, C. et al. (2008b). Control of the
temporal interplay between
excitation and inhibition by the statistics of visual
input: A V1 network modelling study. Vol. Soc. Neurosci. Abstr. (p.
366.5/II10).
|
|
Kremkow, J., Perrinet, L., Masson,
G. S., & Aertsen, A. (2009). Functional consequences of correlated
excitation and inhibition
on single neuron integration and signal propagation
through synfire chains. Proceedings of the 32nd Göttingen
Neurobiology Conference T26-6B.
|
|
Kuhn, A., Aertsen, A., &
Rotter S. (2004). Neuronal integration of synaptic input in the
fluctuation-driven regime. Journal of Neuroscience, 24(10),
2345–2356.
|
|
Kumar, A., Rotter, S., &
Aertsen, A. (2008a). Conditions for propagating synchronous spiking and
asynchronous firing rates
in a cortical network model. Journal of
Neuroscience, 28(20), 5268–5280.
|
|
Kumar, A., Schrader, S., Aertsen,
A., & Rotter, S. (2008b). The high-conductance state of cortical
networks. Neural Computation, 20(1), 1–43.
|
|
Kumbhani, R. D., Nolt, M. J.,
& Palmer, S. E., (2007). Precision, reliability, and
information-theoretic analysis of visual
thalamocortical neurons. Journal of
Neurophysiology, 98(5), 2647–2663.
|
|
Lampl, I., Reichova, I., &
Ferster, D. (1999). Synchronous membrane potential fluctuations in
neurons of the cat visual cortex.
Neuron, 22(2), 361–374.
|
|
Litvak, V., Sompolinsky, H.,
Segev, I., & Abeles, M. (2003). On the transmission of rate code in
long feedforward networks
with excitatory-inhibitory balance. Journal of
Neuroscience, 23(7), 3006–3015.
|
|
Mainen, Z. F., & Sejnowski, T.
J., (1995). Reliability of spike timing in neocortical neurons. Science,
268(5216), 1503–1506.
|
|
Marre, O., Baudot, P., Levy, M.,
& Frégnac, Y. (2005). High timing precision and reliability, low
redundancy and low entropy
code in V1 neurons during visual processing of natural
scenes. Society for Neuroscience Abstracts, 31, 285.5.
|
|
Mehring, C., Hehl, U., Kubo, M.,
Diesmann, M., & Aertsen, A. (2003). Activity dynamics and
propagation of synchronous spiking
in locally connected random networks. Biological
Cybernetics, 88(5), 395–408.
|
|
Molnár, G., Oláh, S., Komlósi, G.,
Füle, M., Szabadics, J., Varga, C., et al. (2008). Complex events
initiated by individual
spikes in the human cerebral cortex. PLoS Biol, 6(9),
e222.
|
|
Morrison, A., Mehring, C., Geisel,
T., Aertsen, A., & Diesmann, M. (2005). Advancing the boundaries of
high-connectivity network
simulation with distributed computing. Neural
Computation, 17(8), 1776–1801.
|
|
Muller, E., Buesing, L., Schemmel,
J., & Meier, K. (2007). Spike-frequency adapting neural ensembles:
Beyond mean adaptation
and renewal theories. Neural Computation, 19(11),
2958–3010.
|
|
Nawrot, M. P., Boucsein, C.,
Molina, V. R., Riehle, A., Aertsen, A., & Rotter, S. (2008).
Measurement of variability dynamics
in cortical spike trains. Journal of Neuroscience
Methods, 169(2), 374–390.
|
|
Nowak, L. G., Azouz, R.,
Sanchez-Vives, M. V., Gray, C. M., & McCormick, D. A. (2003).
Electrophysiological classes of cat
primary visual cortical neurons in vivo as
revealed by quantitative analyses. Journal of Neurophysiology, 89(3),
1541–1566.
|
|
Okun, M., & Lampl, I. (2008).
Instantaneous correlation of excitation and inhibition during ongoing
and sensory-evoked activities.
Nature Neuroscience, 11(5), 535–537.
|
|
Pinto, D. J., Hartings, J. A.,
Brumberg, J. C., & Simons, D. J. (2003). Cortical damping: Analysis
of thalamocortical response
transformations in rodent barrel cortex. Cerebral
Cortex, 13(1), 33–44.
|
|
Pouille, F., & Scanziani, M.
(2001). Enforcement of temporal fidelity in pyramidal cells by somatic
feed-forward inhibition.
Science, 293(5532), 1159–1163.
|
|
Povysheva, N. V., Gonzalez-Burgos,
G., Zaitsev, A. V., Kröner, S., Barrionuevo, G., Lewis, D. A., &
Krimer, L. S. (2006).
Properties of excitatory synaptic responses in
fast-spiking interneurons and pyramidal cells from monkey and rat
prefrontal
cortex. Cerebral Cortex, 16(4), 541–552.
|
|
Rudolph, M., Pospischil, M.,
Timofeev, I., & Destexhe, A. (2007). Inhibition determines membrane
potential dynamics and controls
action potential generation in awake and sleeping cat
cortex. Journal of Neuroscience, 27(20), 5280–5290.
|
|
Schrader, S., Morrison, A., &
Diesmann, M. (2007). A composition machine for complex movements. Proceedings
of the 31st Göttingen Neurobiology Conference TS18-1C.
|
|
Shadlen, M. N., & Newsome, W.
T. (1994). Noise, neural codes and cortical organization. Current
Opinion in Neurobiology, 4(4), 569–579.
|
|
Shadlen, M. N., & Newsome, W.
T. (1998). The variable discharge of cortical neurons: Implications for
connectivity, computation,
and information coding. Journal of Neuroscience, 18(10),
3870–3896.
|
|
Silberberg, G., & Markram, H.
(2007). Disynaptic inhibition between neocortical pyramidal cells
mediated by martinotti cells.
Neuron, 53(5), 735–746.
|
|
Smith, M., & Kohn, A. (2008).
Spatial and temporal scales of neuronal correlation in primary visual
cortex. Journal of Neuroscience, 28(48), 12591–12603.
|
|
Somers, D. C., Nelson, S. B.,
& Sur, M. (1995). An emergent model of orientation selectivity in
cat visual cortical simple
cells. Journal of Neuroscience, 15(8),
5448-5465.
|
|
Stepanyants, A., Hirsch, J.,
Martinez, L. M., Kisvárday, Z. F., Ferecskó, A. S., & Chklovskii,
D-B. (2008). Local potential
connectivity in cat primary visual cortex. Cerebral
Cortex, 18(1), 13–28.
|
|
Swadlow, H. A. (2003). Fast-spike
interneurons and feedforward inhibition in awake sensory neocortex. Cerebral
Cortex, 13(1), 25–32.
|
|
Tetzlaff, T., Geisel, T., &
Diesmann, M. (2002). The ground state of cortical feed-forward networks.
Neurocomputing, 44–46, 673–678.
|
|
Thomson, A. M., West, D. C., Wang,
Y., & Bannister, A. P. (2002). Synaptic connections and small
circuits involving excitatory
and inhibitory neurons in layers 2–5 of adult rat and
cat neocortex: Triple intracellular recordings and biocytin labelling
in vitro. Cerebral Cortex, 12(9),
936–953.
|
|
Tiesinga, P., Fellous, J.-M.,
& Sejnowski, T. J. (2008). Regulation of spike timing in visual
cortical circuits. Nature Reviews. Neuroscience, 9(2), 97–107.
|
|
Troyer, T. W., Krukowski, A. E.,
Priebe, N. J., & Miller, K. D. (1998). Contrast-invariant
orientation tuning in cat visual
cortex: Thalamocortical input tuning and
correlation-based intracortical connectivity. Journal of
Neuroscience, 18(15), 5908–5927.
|
|
Tucker, T. R., & Katz, L. C.
(2003a). Recruitment of local inhibitory networks by horizontal
connections in layer 2/3 of ferret
visual cortex. Journal of Neurophysiology, 89(1),
501–512.
|
|
Tucker, T. R., & Katz, L. C.
(2003b). Spatiotemporal patterns of excitation and inhibition evoked by
the horizontal network
in layer 2/3 of ferret visual cortex. Journal of
Neurophysiology, 89(1), 488–500.
|
|
van Vreeswijk, C., &
Sompolinsky, H. (1996). Chaos in neuronal networks with balanced
excitatory and inhibitory activity.
Science, 274(5293), 1724–1746.
|
|
Vogels, T. P., & Abbott, L. F.
(2009). Gating multiple signals through detailed balance of excitation
and inhibition in spiking
networks. Nature Neuroscience, 12(4), 483–491.
|
|
Wehr, M. S., & Zador, A. M.
(2003). Balanced inhibition underlies tuning and sharpens spike timing
in auditory cortex. Nature, 426(6965), 442–446.
|
|
Yger, P., Bruderle, D., Eppler,
J., Kremkow J., Pecevski, D., Perrinet, L., et al. (2009).
NeuralEnsemble: Towards a meta-environment
for network modeling and data analysis. Eight
Göttingen Meeting of the German neuroscience society (pp. T26–4C). http://www.incm.cnrs-mrs.fr/LaurentPerrinet/Publications/Yger09gns.
|
|
|
|