The Stroop effect involves an excitatory–inhibitory fronto-cerebellar loop

Abstract

The Stroop effect is a classical, well-known behavioral phenomenon in humans that refers to robust interference between language and color information. It remains unclear, however, when the interference occurs and how it is resolved in the brain. Here we show that the Stroop effect occurs during perception of color–word stimuli and involves a cross-hemispheric, excitatory–inhibitory loop functionally connecting the lateral prefrontal cortex and cerebellum. Participants performed a Stroop task and a non-verbal control task (which we term the Swimmy task), and made a response vocally or manually. The Stroop effect involved the lateral prefrontal cortex in the left hemisphere and the cerebellum in the right hemisphere, independently of the response type; such lateralization was absent during the Swimmy task, however. Moreover, the prefrontal cortex amplified cerebellar activity, whereas the cerebellum suppressed prefrontal activity. This fronto–cerebellar loop may implement language and cognitive systems that enable goal-directed behavior during perceptual conflicts.

Introduction
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It is widely accepted that the brain regions responsible for cognitive and language functions are associative neocortical regions distributed in the cerebrum17,18,30,39. Increasing evidence suggests that the cerebellum also plays important roles in language and cognitive control40,41,42,43,44,45,46,47,48,49. This cerebellar involvement is associated with dorsal regions in the lateral hemispheres (crus I/II, lobules VI/VIIb)41,45,46, and is independent of sensorimotor functions implicated in rostral and caudal ventromedial regions (lobules I-VI, VIIIa/b)41,50,51. These cerebellar regions constitute a cortico-cerebellar loop between cerebral cortical regions in the contra-lateral hemisphere41,44,50,51 (Fig. 1b). Importantly, damage to the dorsolateral cerebellar regions impairs language functions41,45,52, and a classical neuroimaging study reported that language processing without vocal response involves a cerebellar region in the right hemisphere52. This collective evidence suggests that a cross-hemispheric cerebro-cerebellar loop is involved in cognitive and language functions (Fig. 1b). Accordingly, we asked whether the cerebellum plays an important role during the resolution of the Stroop effect involving cognitive and language processing.
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Discussion

The current study examined the neural mechanisms underlying the Stroop effect by manipulating the verbality of the stimulus to be perceived and the response to be made. The resolution of Stroop interference involved the left lateral prefrontal cortex and right cerebellum, but the lateralized involvement was not observed in the non-verbal control task (Fig. 8a). Resolution of the interference by fronto-cerebellar processes involved excitatory signaling from the prefrontal to cerebellar regions and inhibitory signaling from the cerebellar to prefrontal regions (Fig. 8b). These findings were unrelated to the verbality of the response generation. Our results suggest that Stroop interference occurs during the perception of language and color information, and is resolved by the coordinated fronto-cerebellar loop that may regulate goal-relevant information.


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One interesting finding regarding the directional functional connectivity observed in this study is that the cerebellum sent inhibitory signals to the prefrontal cortex, whereas the prefrontal cortex sent excitatory signals to the cerebellum, a pattern that was enhanced in the incongruent trials (Figs. 3c and 8b). In the cortico-cerebellar loop, Purkinje cells receive excitatory projections from granule cells within the cerebellar cortex, and send inhibitory projections to the deep cerebellar nuclei, which send signals to the thalamus toward neocortical regions41,44,51 (Fig. 8c). Importantly, the inhibitory projections of the Purkinje cells constitute only one output from the cerebellar cortex. Thus, the inhibitory signals from the cerebellum to the prefrontal cortex observed in our study may reflect the functionality of the Purkinje cells within the cerebro-cerebellar loop (Fig. 8c), although strong fMRI signals in the cerebellum do not reflect Purkinje cell activity alone, and may reflect other neuronal activity of granule cells41,86. As such, the strong inhibitory signaling from the cerebellum to the prefrontal cortex may help to filter out task-irrelevant signals derived from visual information that interfered with appropriate task performance in the incongruent trials (Fig. 8c).
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A key question in this study is how the Stroop effect occurs and is resolved in the brain. This question concerns not only neural correlates (i.e., where in the brain), but also task-related signal processing (i.e., what signals are in the brain). For the former, we performed exploratory analysis across the brain and identified multiple brain regions, including the lPFC and cerebellum. For the latter, we performed directional functional connectivity analysis based on DCM and found inhibitory–excitatory signaling between the lPFC and cerebellum. As such, this study provided neurophysiological evidence to answer the question.
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Link zur Studie bei Nature.com