Abstract
Electrophysiological and functional neuroimaging findings indicate that the neural mechanisms underlying the processing of emotional dimensions (i.e., valence, arousal) constitute a spatially and temporally distributed emotional network, modulated by the arousal and/or valence of the emotional stimuli. We examined the time course and source distribution of gamma time-locked magnetoencephalographic activity in response to a series of emotional stimuli viewed by healthy adults. We used a beamformer and a sliding window analysis to generate a succession of spatial maps of event-related brain responses across distinct levels of valence (pleasant/unpleasant) and arousal (high/low) in 30–100 Hz. Our results show parallel emotion-related responses along specific temporal windows involving mainly dissociable neural pathways for valence and arousal during emotional picture processing. Pleasant valence was localized in the left inferior frontal gyrus, while unpleasant valence in the right occipital gyrus, the precuneus, and the left caudate nucleus. High arousal was processed by the left orbitofrontal cortex, amygdala, and inferior frontal gyrus, as well as the right middle temporal gyrus, inferior parietal lobule, and occipital gyrus. Pleasant by high arousal interaction was localized in the left inferior and superior frontal gyrus, as well as the right caudate nucleus, putamen, and gyrus rectus. Unpleasant by high arousal interaction was processed by the right superior parietal gyrus. Valence was prioritized (onset at ∼60 ms) to all other effects, while pleasant valence was short lived in comparison to unpleasant valence (offsets at ∼110 and ∼320 ms, respectively). Both arousal and valence × arousal interactions emerged relatively early (onset at ∼150 ms, and ∼170 ms, respectively). Our findings support the notion that brain regions differentiate between valence and arousal, and demonstrate, for the first time, that these brain regions may also respond to distinct combinations of these two dimensions within specific time windows.
Highlights
Neuroimaging and electrophysiological studies contributed to debates over the nature and function of emotion refining our understanding of how the human brain generates and represents emotions
We examined with magnetoencephalography (MEG) the responses of two brain structures as a function of valence and arousal (Russell, 1980): amygdala (Styliadis et al, 2014) which is well-known to be involved in emotional processing, and cerebellum (Styliadis et al, 2015) which is a recent addition to our classical view of the emotion-related distributed circuitry (Adamaszek et al, 2017)
We found that: (i) valence and arousal are represented by mainly dissociable neural substrates; (ii) some brain regions [inferior frontal gyrus (IFG)] respond independently to both valence and arousal; and (iii) these neuronal representations unfold in parallel along distinct temporal streams, which depend on valence and arousal
Summary
Neuroimaging and electrophysiological studies contributed to debates over the nature and function of emotion refining our understanding of how the human brain generates and represents emotions. Leaving aside different theories regarding the most appropriate and meaningful conceptualization of emotions (Barrett, 2006; Mauss and Robinson, 2009), neuroscientists converge on the notion that emotional processing involves multiple interrelating brain regions (Lindquist et al, 2012). Though these spatial patterns can overlap for the processing of different emotional stimuli, their associated temporal signature is considered unique (Esslen et al, 2004; Costa et al, 2014; Waugh et al, 2015). We are motivated by these studies to fill a similar knowledge gap for the spatiotemporal evolution of emotion in terms of valence and arousal
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