Verifications and implications of the MEG Sources by the fMRI Study

Based on the peak values of ABA in the expectation interval (Figure 3-12), we introduced a face-identity-predictive (FIP) network including (Figure 4-2). The FIP network comprises brain areas related to (1) early vision, like the cuneus that we referred to the secondary visual area V2, (2) early face recognition like the occipital face area (OFA) (Pitcher et al., 2011) and (3) brain areas that have been related to perceptual closure processes like the lateral occipital cortex (LOC) (Grill-Spector et al., 2001; Grutzner et al., 2010). Further, the FIP network comprises brain areas related to memory functions like the (4) precuneus (PreC) in the left and right hemispheres and (5) the parahippocampal gyrus (PHC).

The follow-up decoding analysis via a sequential classification approach (SCA) revealed a sequence of six sources which were, according to the SCA procedure, ordered by relevance: PHC, OFA, right PreC, V2, LOC and left PreC. Looking at the effect size (ES) a similar pattern was observed: A medium ES was registered for the first three voxels and a small one or less for the others. Even if all sources were respected, this tentatively suggests that the PHC, the OFA and the precuneus, that is to say the first three sources of the sequence, were probably the more relevant sources.

Further, three sources (OFA, LOC and PreC) were more or less verified by the fMRI study. While conducting the fMRI study, we expected to gain further insights into the mapping of the expectation interval in the assumption of a positive relationship of ABA and BOLD response. Considering the relationship between the electro-physiological frequencies band activity and BOLD responses, the literature refers to two main findings. First, higher frequencies are better correlated than lower frequencies (Niessing et al., 2005; Scheeringa et al., 2016). Second, most studies that report high correlation of ABA and BOLD response posit a negative relationship between ABA and BOLD and show decreasing post-stimulus-related ABA (Goldman et al., 2002; Hall et al., 2014; Laufs et al., 2003; Scheeringa et al., 2011, 2016; Winterer et al., 2007; Zumer et al., 2010). Some exist which report positive relationships between ABA and BOLD response (Gonçalves et al., 2006; Jann et al., 2009; Mayhew et al., 2013). For most of these studies it applies that these refer to resting state recordings (Mayhew et al., 2013). Interestingly, Liu and colleagues (Liu et al., 2012) report the relationship of deep brain (thalamic) ABA to be positive correlated to posterior BOLD responses. This evidence illustrates that both measures of the same mechanisms (expectation of the TFID) do not have to show the same spatial activation pattern, rather indicate that the measures capture a different brain signal. Considering this, the relationship between the different brain activity captured by MEG and the fMRI will shed more light into this.

Briefly, the MEG signal is mainly caused by the primary current, whereas the source of the primary current is the excitatory postsynaptic potential in pyramidal neurons of the cerebral cortex (Onozuka and Yen, 2008). Thus, the MEG signal can be interpreted as a direct signal of neuronal function. Not that simple it is for the BOLD signal.

Figure 4-2: Outline of the face-Identity-predictive (FIP) network. The outline represents the network determined by investigating the alpha frequency band activity (ABA) in the expectation interval. Each brain area is indicated by a superficial (layer 2/3) and deep pyramid (layer 5/6) cells and intermediate stellate cells (layer 4). The layer-intrinsic wiring is abstracted by a dotted circular flow, for more details, see the Introduction and Figure 1-2. The FIP network illustrated here is proposed to represent the internal model. According to Bastos and colleagues (Bastos et al., 2012), ABA represents top-down influences, thus, upon the anatomical connections we illustrated feedback connections between the brain regions by a black arrow conveying predictions top-down. We illustrated feedforward connections by dotted pale red arrows upon anatomical evidence (Felleman et al., 1991). Feedforward connections project onto stellar cells. Feeback connections project onto superficial and deep layer neurons but terminate in the superficial layers, because deep layer pyramid cells have dendrites reaching to the superficial layers.

Seminal work was done by Logothetis and colleagues who described that the BOLD signal captures LFP and multi-unit activity (Logothetis et al., 2001) but also synaptic modulatory activity (Logothetis, 2002). Logothetis (Logothetis, 2002) explained BOLD responses in V4 during motion perception by anatomical descending connections from MT which might be of modulatory function. Thus, the BOLD response in V4 referred to synaptic activity in V4 with its origins in MT. This evidence is in line with the PCT that top-down influence is

associated with a modulatory effect in lower cortical brain regions, especially when it comes to the precision of the prediction (Kanai et al., 2015). Considering this, the BOLD response observed in the ventral stream could possibly refer to synaptic activity which originates in sources captured by brain areas located at the top of the hierarchy like the PHC and the precuneus located by the ABA. Further support for this is that early sensory brain areas receive top-down predictions to prepare for post-stimulus processing reported by Bauer and Colleagues (Bauer et al., 2014). In the case of the FIP network this preparatory function might apply to the PHC which is part of a large network connecting frontal and parietal brain areas but also temporal and occipital regions (Aminoff et al., 2013) but also preparatory function might apply to the PreC.

Alternatively, the brain areas revealed by the BOLD signal may be associated to a slightly different brain mechanism because of a much broader time window captured by fMRI compared to MEG. In other words, the differences captured by the fMRI might be due to the low time resolution of the fMRI. This is supported by the left brain activity in the occipital fusiform gyrus. Bi and colleagues (Bi et al., 2014) reported left brain posterior brain activity during learning of facial identity. They argue that the left fusiform cortex is more susceptible to perceptual learning and more plastic. As a result, the left fusiform cortex is open to changes and better able to adapt to these changes in the dynamic visual world, and in contrast the right fusiform cortex is fixed in the mature brain in its function (Golarai et al., 2007). Thus, we conclude that at least these left brain regions captured by the BOLD signal and not by the ABA may correspond to the perceptual learning mechanisms.

Summarizing this, the predictive brain sampled by the BOLD response and the ABA revealed same overlapping and not overlapping brain regions. The OFA in both measures overlaps by close voxels surrounding the peak voxels. The other brain regions do not overlap but are closely neighbouring each other; these are the left PreC, the LOC and the cuneal/V2 activity. A brain region hardly detected by the BOLD signal was the PHC. Among all six brain regions, the PHC was determined as one of the highest in the hierarchy. Because this region was considered as one of the brain areas of higher relevance, this is in line with earlier studies that the BOLD response might capture synaptic top-down modulatory activity, rather than local activity.