Predictive coding in visual search as revealed by cross-frequency EEG phase synchronization

Our experience, memories, and knowledge have modulatory influence on how we perceive the world. Top-down expectancies are supposed to be implemented as templates in our minds. Mental templates are compared against the current sensory input, which can match or mismatch with the aim of minimizing prediction error (Friston, 2005). But what are the underlying neuronal mechanisms leading to the activation of mental templates and their comparison with sensory input, i.e., predictive coding? Biasing sensory processing by expectancies has been strongly associated with prefrontal brain activity influencing responses in visual cortex (e.g., Summerfield et al., 2006; Olivers et al., 2011; Spaak et al., 2015). Moreover, electrophysiological evidence gathered in patients with prefrontal cortex lesions (Yago et al., 2004) suggests that the prefrontal cortex acts with excitatory drive on extrastriate cortex within three time windows during template matching in visual attention tasks: as early as 100 ms after target onset through selection of spatial locations; during the analysis of non-spatial features of attended objects around 250 ms after target onset; and in a later phase around 300 ms during which discrimination and template matching occur. This recurrent prefrontal drive on higher visual areas can be interpreted as top-down reactivation of target memory traces, thus, the activation of a mental template that needs to be compared to visual input (Desimone and Duncan, 1995). A common way of analysing interregional transfer of neural signals in the human brain is by means of coherent oscillatory brain activity. Rhythmical brain activity as recorded with the electroencephalogram (EEG) is an indicator for locally highly synchronized neuronal activity. If two distant brain areas are functionally coupled, it is assumed that a higher level of coherent, synchronous neuronal activity can be found between these distant areas than one would expect from chance. Comprehensive work by von Stein and co-workers suggests that long-range interaction between prefrontal and posterior cortices necessary in top-down control of cognitive processes is reflected by neural activity resonating in large-scale networks and therefore oscillating at rather slow frequencies: so called theta and alpha oscillations (von Stein et al., 1999, 2000; von Stein and Sarnthein, 2000). In humans, coherent, synchronous prefrontal to parietal brain oscillatory activity particularly in slower frequency bands (around 5 and 10 Hz) has been observed when a high level of top-down activity is necessary in a range of different visual tasks (see Sauseng and Klimesch, 2008; Sauseng et al., 2010 for reviews). Long-range communication in the monkey brain has also been attributed to rather slow oscillatory activity (in the theta and delta frequency range) whereas it has been suggested that local, fast rhythmical cortical activity (in the gamma frequency band) is associated more strongly with bottom-up visual processing (Bruns and Eckhorn, 2004; Eckhorn et al., 2004; Bastos et al., 2015; Zheng and Colgin, 2015).