Network-state modulation of power-law frequency-scaling in visual cortical neurons.
Sami El Boustani, Olivier Marre, Séebastien Béhuret, Pierre Baudot, Pierre Yger, Thierry Bal, Alain Destexhe and Yves Frégnac
PLoS Computational Biology 5: e1000519, 2009.
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Abstract
Various types of neural-based signals, such as EEG, local field potentials and intracellular synaptic potentials, integrate multiple sources of activity distributed across large assemblies. They have in common a power-law frequency-scaling structure at high frequencies, but it is still unclear whether this scaling property is dominated by intrinsic neuronal properties or by network activity. The latter case is particularly interesting because if frequency-scaling reflects the network state, it could be used to characterize the functional impact of the connectivity. In intracellularly-recorded neurons of cat primary visual cortex in vivo, the power spectral density of Vm activity displays a power-law structure at high frequencies, with a fractional scaling exponent. We show that this exponent is not constant, but depends on the visual statistics used to drive the network. To investigate the determinants of this frequency-scaling, we considered a generic recurrent model of cortex, receiving a retinotopically organized external input. Similarly to the in vivo case, our in computo simulations show that the scaling exponent reflects the correlation level imposed in the input. This systematic dependence was also replicated at the single cell level, by controlling independently, in a parametric way, the strength and the temporal decay of the pairwise correlation between presynaptic inputs. This last model was implemented in vitro by imposing the correlation control in artificial presynaptic spike trains through dynamic-clamp techniques. These in vitro manipulations induced a modulation of the scaling exponent, similar to that observed in vivo and predicted in computo. We conclude that the frequency-scaling exponent of the Vm reflects stimulus-driven correlations in the cortical network activity. Therefore we propose that the scaling exponent could be used to read-out the “effective” connectivity responsible for the dynamical signature of the population signals measured at different integration levels, from Vm to LFP, EEG and fMRI.
Authors’ summary
Intracellular recording of neocortical neurons provides an opportunity of characterizing the statistical signature of the synaptic bombardment to which it is submitted. Indeed the membrane potential displays intense fluctuations which reflect the cumulative activity of thousand of input neurons. In sensory cortical areas, this measure could be used to estimate the correlational structure of the external drive. We show that changes in the statistical properties of network activity, namely the local correlation between neurons, can be detected by analyzing the power spectrum density (PSD) of the subthreshold membrane potential. These PSD can be fitted by a power-law function 1/falpha in the upper temporal frequency range. In vivo recordings in primary visual cortex show that the alpha exponent varies with the statistics of the sensory input. Most remarkably, the exponent observed in the ongoing activity is indistinguishable from that evoked by natural visual statistics. These results are emulated by models which demonstrate that the exponent alpha is determined by the local level of correlation imposed in the recurrent network activity. Similar relationships are also reproduced in cortical neurons recorded in vitro with artificial synaptic inputs by controlling in computo the level of correlation in real time.
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