The SCP is not specific enough to represent conscious content.

He and Raichle [1xSee all References[1] persuasively argue that slow cortical potentials (SCP), the local field potential (LFP) below 1 Hz, is generated by long-lasting depolarization in the apical dendrites of superficial cortical pyramidal cells and that the SCP is closely related to fMRI signals. They propose that the SCP ‘might contribute directly to the emergence of consciousness’. They point to a number of experiments in which a relationship between SCPs and conscious perception has been experimentally established. Their ingenious proposal can be criticized, however, on several grounds.First, it is unclear whether the SCP is causal or an epiphenomenon with regard to consciousness. That is, is it the existence of the SCP per se that carries the specific content of consciousness that is subjectively experienced or is it the activity of the associated pyramidal cells that is responsible for the experience? In principle, clever biophysical experiments that manipulate the extracellular resistivity, combined with targeted opto-genetic techniques that induce post-synaptic depolarization [2xParvalbumin neurons and gamma rhythms enhance cortical circuit performance. Sohal, V.S. et al. Nature. 2009; 490: 698–702Crossref | Scopus (826)See all References[2] could dissociate activity in the pyramidal cells from generation of the slow changes in the local field potential.The most significant objection against the idea that SCP or related bulk measures are causally involved with conscious content (as compared to often correlating with such content) is the incredible specificity of perception – think of every frame in every movie that was ever produced or that will ever be produced; each one corresponds to a discrete visual experience. This informational richness requires a neuronal substrate that is equally specific. The physics of cortical tissue, however, limits the specificity of the LFP: the SCP, like any other aspect of the LFP, is generated by the linear superposition of ohmic current flow from all sinks and sources (scaled inversely by distance) in a particular volume [3xEstimation of population firing rates and current source densities from laminar electrode recordings. Pettersen, K.H. et al. J. Comput. Neurosci. 2008; 24: 291–313Crossref | PubMed | Scopus (38)See all References[3]. This summation is not conducive to high informational content. It is extremely unlikely that the content of any one experience is encoded in any part of the LPF. Conversely, individual neurons in the human brain do represent very specific percepts, such as the sight or the name of a particular celebrity [4xInvariant visual representation by single neurons in the human brain. Quian Quiroga, R. et al. Nature. 2005; 435: 1102–1107Crossref | PubMed | Scopus (626)See all References[4]. Thus, it is to specific groups of neurons and to their activity patterns and their myriad of causal interactions that we must look for causes of consciousness [5xConsciousness as integrated information: a provisional manifesto. Tononi, G. Biol. Bull. 2008; 215: 216–242Crossref | PubMedSee all References[5].Furthermore, He and Raichle [1xSee all References[1] hypothesize that pyramidal cells in layers 5 and 6 ‘provide specialized local processing that assist superficial-layer computations and send output to subcortical structures’. It is difficult to believe that the massive cortico-thalamic feed-forward and feed-back connections [6xWhy is there a hierarchy of visual cortical and thalamic areas: The no-strong loops hypothesis. Crick, F.C. and Koch, C. Nature. 1998; 391: 245–249Crossref | PubMed | Scopus (210)See all References[6] as well as so many cortico-cortical feedback connections, all of which are located in the deep layers, have no direct role to play in consciousness.He and Raichle [1xSee all References[1] also state that ‘This hypothesis, unlike several previous theories of consciousness, is firmly rooted in physiology and as such is entirely amenable to empirical testing’. The introduction of the idea of neuronal correlates of consciousness [7xTowards a neurobiological theory of consciousness. Crick, F.C. and Koch, C. Seminar in the Neurosciences. 1990; 2: 263–275CrossrefSee all References[7] – here synchronized oscillations in the 40 Hz range in subsets of cortical neurons – as well as global neuronal workspace theory [8xA neuronal network model linking subjective reports and objective physiological data during conscious perception. Dehaene, S. et al. Proc. Natl. Acad. Sci. U.S.A. 2003; 100: 8520–8525Crossref | PubMed | Scopus (367)See all References[8] are both firmly rooted in physiology and are being empirically tested.Finally, in defense of insects and other invertebrates. Unlike mammals, their brains are not organized into multi-layered sheets of neurons; yet they employ similar principles of information representation, including slow oscillations (e.g. 0.69 Hz; [9xOdour-modulated collective network oscillations of olfactory interneurons in a terrestrial mollusk. Gelperin, A. and Tank, D.W. Nature. 1990; 345: 437–440Crossref | PubMed | Scopus (163)See all References[9]), sparse single neuron coding, and neuronal densities in structures like the mushroom body that are ten times bigger than in neocortex with a high but unknown degree of synaptic integration. Given the multi-faceted and adaptive behavior of insects, they too might possess some measure of consciousness and they too might experience the sights and sounds of life [10xSee all References[10].