Distinct cerebellar lobules process arousal, valence and their interaction in parallel following a temporal hierarchy

The cerebellum participates in emotion-related neural circuits formed by different cortical and subcortical areas, which sub-serve arousal and valence. Recent neuroimaging studies have shown a functional specificity of cerebellar lobules in the processing of emotional stimuli. However, little is known about the temporal component of this process. The goal of the current study is to assess the spatiotemporal profile of neural responses within the cerebellum during the processing of arousal and valence. We hypothesized that the excitation and timing of distinct cerebellar lobules is influenced by the emotional content of the stimuli. By using magnetoencephalography, we recorded magnetic fields from twelve healthy human individuals while passively viewing affective pictures rated along arousal and valence. By using a beamformer, we localized gamma-band activity in the cerebellum across time and we related the foci of activity to the anatomical organization of the cerebellum. Successive cerebellar activations were observed within distinct lobules starting ~160ms after the stimuli onset. Arousal was processed within both vermal (VI and VIIIa) and hemispheric (left Crus II) lobules. Valence (left VI) and its interaction (left V and left Crus I) with arousal were processed only within hemispheric lobules. Arousal processing was identified first at early latencies (160ms) and was long-lived (until 980ms). In contrast, the processing of valence and its interaction to arousal was short lived at later stages (420-530ms and 570-640ms respectively). Our findings provide for the first time evidence that distinct cerebellar lobules process arousal, valence, and their interaction in a parallel yet temporally hierarchical manner determined by the emotional content of the stimuli.