Efficient neural codes can lead to spurious synchronization

Abstract

Experimental and computational evidence shows that cognitive function requires an optimal balance between global integrative and local functionally specialized processes (Tononi et al., 1998). This balance can be described in terms of transient short-lived episodes of synchronized activity between different parts of the brain (Friston, 2000; Breakspear, 2002). Synchronization over multiple frequency bands is thought to subserve fundamental operations of cortical computation (Varela et al., 2001; Fries, 2009), and to be one of the mechanisms mediating the large-scale coordination of scattered functionally specialized brain regions. For instance, transient synchronization of neuronal oscillatory activity in the 30–80 Hz range has been proposed to act as an integrative mechanism, binding together spatially distributed neural populations in parallel networks during sensory perception and information processing (Singer, 1995; Miltner et al., 1999; Rodriguez et al., 1999). More generally, synchrony may subserve an integrative function in cognitive functions as diverse as motor planning, working or associative memory, or emotional regulation (Varela, 1995). Over the past 15 years, cognitive neuroscientists have tried to capture and quantify neural synchronies across distant brain regions both during spontaneous brain activity and in association with the execution of a wide range of cognitive tasks, using neuroimaging techniques such as functional resonance imaging, electro- or magneto-encephalography. Theoretical advances in various fields including non-linear dynamical systems theory have allowed the study of various types of synchronization from time series (Pereda et al., 2005), and to address important issues such as determining whether observed couplings do not reflect a mere correlation between activities recorded at two different brain regions but rather a causal relationship (Granger, 1969) whereby a brain region would cause the activity of the other one. However, not all measured synchrony may in fact represent neurophysiologically and cognitively relevant computations: various confounding effects may mislead into identifying functional connectivity, defined as the temporal correlations between spatially remote neurophysiological events, with effective connectivity, i.e., the influence one neuronal system exerts over another (Friston, 1994). For instance, measured synchrony may stem from common thalamo-cortical afferents or neuromodulatory input from ascending neurotransmitter systems, or may be the visible part of indirect effective connectivity. Other technique-specific artifactual sources of synchrony, for instance induced by volume conduction, are also well-known to cognitive neuroscientists (Stam et al., 2007). Here, we address a further (extra-cranial) confounding source: the appearance of simultaneous, yet uncorrelated stimuli. We show how the activity of two groups of binary neurons, whose output code is optimized to represent rare events with short codes, can exhibit a synchronization when such rare events appear, even in the absence of shared information or common computational activities.