Sensitivity to perturbations in vivo implies high noise and suggests rate coding in cortex

Abstract

Neural responses are variable — identical sensory stimuli produce different responses — but it is not clear whether this variability carries important information, or whether it is just noise. London et al. characterize the sensitivity to small fluctuations of in vivo cortical networks in rat barrel cortex in the context of their consequences for neural coding. A perturbation equivalent to adding a single spike in one neuron produces about 28 additional spikes in its projection targets and a detectable increase in local firing rate. Simulations suggest that this amplification leads to large intrinsic variations in the system that are pure noise, carrying no information about the input, and therefore unsuited for carrying a reliable temporal code. The authors conclude that rat barrel cortex is likely to use primarily a rate code. Neural responses are variable, but it is unclear whether this variability carries important information or is just noise. Here the authors characterize the sensitivity to small fluctuations of in vivo cortical networks in rat barrel cortex in the context of neural coding, finding that perturbations are amplified and cause an increase in local firing rate. Simulations suggest that this amplification leads to variations in the system that are pure noise and, therefore, unsuited for carrying a reliable temporal code. It is well known that neural activity exhibits variability, in the sense that identical sensory stimuli produce different responses1,2,3, but it has been difficult to determine what this variability means. Is it noise, or does it carry important information—about, for example, the internal state of the organism? Here we address this issue from the bottom up, by asking whether small perturbations to activity in cortical networks are amplified. Based on in vivo whole-cell patch-clamp recordings in rat barrel cortex, we find that a perturbation consisting of a single extra spike in one neuron produces approximately 28 additional spikes in its postsynaptic targets. We also show, using simultaneous intra- and extracellular recordings, that a single spike in a neuron produces a detectable increase in firing rate in the local network. Theoretical analysis indicates that this amplification leads to intrinsic, stimulus-independent variations in membrane potential of the order of ±2.2–4.5 mV—variations that are pure noise, and so carry no information at all. Therefore, for the brain to perform reliable computations, it must either use a rate code, or generate very large, fast depolarizing events, such as those proposed by the theory of synfire chains4,5. However, in our in vivo recordings, we found that such events were very rare. Our findings are thus consistent with the idea that cortex is likely to use primarily a rate code.