Intracellular and computational evidence for a dominant role of internal network activity in cortical computations

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The mammalian cerebral cortex is characterized by intense spontaneous activity, depending on brain region, age, and behavioral state. Classically, the cortex is considered as being driven by the senses, a paradigm which corresponds well to experiments in quiescent or deeply anesthetized states. In awake animals, however, the spontaneous activity cannot be considered as ‘background noise’, but is of comparable  or even higher  amplitude than evoked sensory responses. Recent evidence suggests that this internal activity is not only dominant, but also it shares many properties with the responses to natural sensory inputs, suggesting that the spontaneous activity is not independent of the sensory input. Such evidence is reviewed here, with an emphasis on intracellular and computational aspects. Statistical measures, such as the spike-triggered average of synaptic conductances, show that the impact of internal network state on spiking activity is major in awake animals. Thus, cortical activity cannot be considered as being driven by the senses, but sensory inputs rather seem to modulate and modify the internal dynamics of cerebral cortex. This view offers an attractive interpretation not only of dreaming activity (absence of sensory input), but also of several mental disorders.

Highlights

► The brain displays considerable spontaneous activity. ► Neurons do not respond only to external inputs, but the response is also a function of the spontaneous activity. ► The paper reviews intracellular and modeling evidence for this phenomenon. ► A scheme is proposed to reconcile apparently conflicting results. ► It is concluded that spontaneous activity should be an integral part of brain computations.

Section snippets

The intrinsic activity of the brain

The first proposal that neurons are not passive relays being driven by external inputs dates back to the early 20th century with the Belgian electrophysiologist Frederic Bremer [16••, 17]. He proposed that neurons generate intrinsic and self-sustained activity under the form of intrinsic oscillatory properties. The current thinking at the time was that oscillatory activity arises from circulating waves of activity, a theory called the ‘circus movement theory’. Bremer was an opponent to this

Is there quiescence in the absence of input?

Although such findings offer a nice perspective to explain population recordings, they are not consistent with all of the available experimental data. In particular, in the primary visual cortex (V1), a large number of studies have demonstrated clear visual responses and selectivity of neurons to features such as orientation, direction, and contract [29]. Not much spontaneous activity seems to be present in such single-cell experiments (see also [30]). Very low levels of spontaneous activity

Intracellular and computational evidence for dominant internal dynamics

Another set of evidence is provided by model-based analyses of intracellular recordings in vivo. Figure 2a shows examples of intracellular recordings of cat V1 neurons during spontaneous activity (SA) and the presentation of natural images (NI) [35] (original data from [36]). To measure statistical similarity, the frequency scaling exponent was computed from the power spectrum of the signals (Figure 2b), yielding exponent values for different stimulus conditions. Remarkably, the exponents were

Proposed scheme to account for the different experiments

To account for the disparity of the above results, a simple model of a neuron receiving two input sources was simulated. First an ‘intrinsic activity’ consisting of stochastic release at excitatory and inhibitory synapses, and second, an ‘external input’ consisting of a controlled stimulation of an independent set of excitatory and inhibitory synapses (see scheme in Figure 5). For weak external inputs, the activity is dominated by intrinsic activity and one recovers the pattern of opposite

Conclusions

In summary, the intracellular and computational results reviewed here collectively suggest that the spike-triggered conductance patterns is a very powerful way to determine whether a system is dominated by its internal activity, or is driven by afferent activity, as summarized in Figure 5. This approach makes a number of predictions, which are briefly discussed here.

First, it suggests that in many sensory systems, the measurements reporting a concerted conductance increase can be explained

References and recommended reading

Papers of particular interest, published within the period of review, have been highlighted as:

  • • of special interest

  • •• of outstanding interest

Acknowledgements

Thanks to Thierry Bal, Olivier Marre, Cyril Monier, Zuzanna Piwkowska, Igor Timofeev, and Yves Frégnac for sharing experimental data, and all members of the UNIC for continuing support. This work has been supported by the CNRS, the Agence Nationale de la Recherche (ANR HR-Cortex) and the European Community (FET grants FACETS FP6-015879, BRAINSCALES FP7-269921).

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