Information theoretic evidence for layer- and frequency-specific changes in cortical information processing under anesthesia

Nature relies on highly distributed computation for the processing of information in nervous systems across the entire animal kingdom. Such distributed computation can be more easily understood if decomposed into the three elementary components of information processing, i.e. storage, transfer and modification, and rigorous information theoretic measures for these components exist. However, the distributed computation is often also linked to neural dynamics exhibiting distinct rhythms. Thus, it would be beneficial to associate the above components of information processing with distinct rhythmic processes where possible. Here we focus on the storage of information in neural dynamics and introduce a novel spectrally-resolved measure of active information storage (AIS). Drawing on intracortical recordings of neural activity under anesthesia before and after loss of consciousness (LOC) we show that anesthesia-related modulation of AIS is highly specific to different frequency bands and that these frequency-specific effects differ across cortical layers and brain regions. We found that in the high/low gamma band the effects of anesthesia result in AIS modulation only in the supergranular layers, while in the alpha/beta band the strongest decrease in AIS can be seen at infragranular layers. Finally, we show that the increase of spectral power at multiple frequencies, in particular at alpha and delta bands in frontal areas, that is often observed during LOC (‘anteriorization’) also impacts local information processing – but in a frequency specific way: Increases in isoflurane concentration induced a decrease in AIS in the alpha frequencies, while they increased AIS in the delta frequency range < 2Hz. Thus, the analysis of spectrally-resolved AIS provides valuable additional insights into changes in cortical information processing under anaesthesia. Author Summary While describing information processing in digital computers is somewhat straightforward and accessible (e.g. how much information is stored in a hard disk or which modification of information a CPU is executing), quantifying the widely distributed information processing in a biological neural system is much more challenging. In neural systems separating the components of distributed information processing - information transfer, storage and modification - helps with this task, but requires accurate mathematical definitions of these components of information processing. These definitions of distributed information processing quantities have become available only very recently. Of the three component processes mentioned above information storage, in particular, has been used with great success to analyze information processing in swarms, and to evolve, and optimize artificial information processing systems. The analysis of information storage has also already proven to be useful for the analysis of biological neural systems. Since in such systems, information processing seems to be often carried out by rhythmic neural activity with different frequencies, a measure of the frequency-specific components of the active information storage is needed. Here introduce such a measure and study how isoflurane anesthesia affects the local information processing in the ferret prefrontal and primary visual areas around loss of consciousness. We found that the modulation of active information storage by isoflurane is specific to frequency, layers and area, and that the analysis of frequency-specific active information storage provides insights not captured by more traditional descriptions of neural activity.