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The fMRI signal, slow cortical potential and consciousness

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As functional magnetic resonance imaging (fMRI) has become a driving force in cognitive neuroscience, it is crucial to understand the neural basis of the fMRI signal. Here, we discuss a novel neurophysiological correlate of the fMRI signal, the slow cortical potential (SCP), which also seems to modulate the power of higher-frequency activity, the more established neurophysiological correlate of the fMRI signal. We further propose a hypothesis for the involvement of the SCP in the emergence of consciousness, and review existing data that lend support to our proposal. This hypothesis, unlike several previous theories of consciousness, is firmly rooted in physiology and as such is entirely amenable to empirical testing.

Introduction

Since its introduction in the early 1990s, functional magnetic resonance imaging (fMRI) has become the most widely used tool in human cognitive neuroscience and has produced a formidable array of brain maps depicting both localization (as in traditional activation studies) and integration (as in more recent functional connectivity studies) of brain activity. Because the fMRI signal measures directly blood oxygenation and only indirectly neuronal activity, an important need for understanding the neural events contributing to the fMRI signal has been widely recognized. Such a need is further stressed by the inconsistencies between several human fMRI and monkey unit physiological studies employing the same tasks [1].

Responding to this need, several studies have compared the fMRI signal (reviewed in Ref. [2]) or its close relatives (including tissue oxygenation [3], blood flow [4] and optical intrinsic signals [5]) with simultaneously recorded electrophysiological signals. The convergent results from these studies suggest that the fMRI signal is contributed predominantly by synaptic activity representing inputs and local processing in an area as measured by local field potentials (LFP) 2, 3, 4, 6, 7. The spiking activity, though often correlated with both the LFP and the fMRI signal, can be dissociated from the latter two in several conditions, including adaptation [8], drug modulation [9], manipulations of excitatory and inhibitory inputs [4] and a spatial separation between input and output activity [7].

Whereas multiple frequency ranges of the LFP (e.g. 5–30 Hz [10], 20–60 Hz 11, 12, ∼25–90 Hz 3, 5, 8, 9, 13) have been correlated with the fMRI signal in different conditions, all of these studies have only assessed power modulations of the LFP because only the power of these frequency ranges has a comparable temporal scale to that of the fMRI signal (< 0.5 Hz). Here, we add a new dimension to this evolving story by bringing in the low-frequency end of field potentials (<4 Hz), which, with a temporal scale overlapping that of the fMRI signal, seems to correlate with the fMRI signal in its raw fluctuations. This signal, termed the ‘slow cortical potential’ (SCP) by us and others 14, 15, 16, seems optimally positioned for carrying out large-scale information integration in the brain. Because conscious experience* is always a unitary and undivided whole 17, 18, segregated information processing in the brain cannot contribute to the conscious awareness of ‘I’. Hence, we propose that the SCP might contribute directly to the emergence of consciousness and review existing empirical evidence supporting this idea. As the current hypothesis is based on a well-defined, well-characterized physiological process, it is entirely amenable to empirical testing.

Section snippets

Evidence for a relationship between the SCP and the fMRI signal

The SCP is the slow end (mainly <1 Hz, can extend up to ∼4 Hz) of the field potential that can be recorded using either depth 19, 20 or surface 15, 21 electrodes (Box 1). Negative shift in surface-recorded SCP indexes increased cortical excitability (for detailed physiology please see the following section). Because the SCP frequency range is subject to artifacts due to sweating (in scalp-electroencephalography [EEG] recordings), movement and electrode drift (if polarizable electrodes are used),

The physiological basis of the SCP

Simultaneous recordings of surface potentials, field potentials in different cortical layers and intracellular membrane potentials have clearly demonstrated that synaptic activities at apical dendrites in superficial layers are the main factor contributing to the SCP. Specifically, long-lasting excitatory postsynaptic potentials (EPSPs) at these apical dendrites underlie negative-going surface-recorded SCPs 14, 19, 31. As an example, we consider the effect of visual stimulation in V1 – a

The SCP and consciousness – a neurophysiological hypothesis of consciousness

From a theoretical perspective, information has to be integrated to contribute to conscious awareness, for conscious experience is always a unitary and undivided whole 17, 18. We suggest that the SCP might be an optimal neural substrate to carry such information integration across wide cortical areas because (i) its slow time scale allows synchronization across long distance despite axonal conduction delays 15, 44, 45, 46; (ii) long-range intracortical and corticocortical connections terminate

Concluding remarks

Studies on the neural basis of the fMRI signal have focused on the LFP power. Here, we present evidence for another neurophysiological signal underlying the fMRI signal that has received much less attention – the SCP. The linkage between the SCP and the fMRI signal not only advances our understanding of cortical physiology but also provides a different vantage point to many experimental results. We further propose that the SCP might carry large-scale information integration in the neocortex

Acknowledgements

We are grateful to Giulio Tononi, Bruno van Swinderen, Avi Snyder, John Zempel, and Harold Burton for insightful discussions. B.J.H. would also like to thank the U.S. Immigration Service under the Bush administration, whose visa background security check forced her to spend two months (following an international conference) in a third country, free of routine obligations—it was during this time that the hypothesis presented herein was initially conjectured. This research was supported by NIH

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