The Distinct Role of the Amygdala, Superior Colliculus and Pulvinar in Processing of Central and Peripheral Snakes

Abstract

IntroductionVisual processing of ecologically relevant stimuli involves a central bias for stimuli demanding detailed processing (e.g., faces), whereas peripheral object processing is based on coarse identification. Fast detection of animal shapes holding a significant phylogenetic value, such as snakes, may benefit from peripheral vision. The amygdala together with the pulvinar and the superior colliculus are implicated in an ongoing debate regarding their role in automatic and deliberate spatial processing of threat signals.MethodsHere we tested twenty healthy participants in an fMRI task, and investigated the role of spatial demands (the main effect of central vs. peripheral vision) in the processing of fear-relevant ecological features. We controlled for stimulus dependence using true or false snakes; snake shapes or snake faces and for task constraints (implicit or explicit). The main idea justifying this double task is that amygdala and superior colliculus are involved in both automatic and controlled processes. Moreover the explicit/implicit instruction in the task with respect to emotion is not necessarily equivalent to explicit vs. implicit in the sense of endogenous vs. exogenous attention, or controlled vs. automatic processes.ResultsWe found that stimulus-driven processing led to increased amygdala responses specifically to true snake shapes presented in the centre or in the peripheral left hemifield (right hemisphere). Importantly, the superior colliculus showed significantly biased and explicit central responses to snake-related stimuli. Moreover, the pulvinar, which also contains foveal representations, also showed strong central responses, extending the results of a recent single cell pulvinar study in monkeys. Similar hemispheric specialization was found across structures: increased amygdala responses occurred to true snake shapes presented to the right hemisphere, with this pattern being closely followed by the superior colliculus and the pulvinar.ConclusionThese results show that subcortical structures containing foveal representations such as the amygdala, pulvinar and superior colliculus play distinct roles in the central and peripheral processing of snake shapes. Our findings suggest multiple phylogenetic fingerprints in the responses of subcortical structures to fear-relevant stimuli.

A Prototypical Template for Rapid Face Detection Is Embedded in the Monkey Superior Colliculus

“…A recent neurophysiological study reported that monkey SC neurons are highly sensitive to stimuli in the foveal VF than previously reported (Chen et al, 2019). Furthermore, fMRI studies reported a similar central bias for faces in the human SC as well as the amygdala in contrast with non-face objects (Almeida et al, 2013(Almeida et al, , 2015. The present results, as well as the previous imaging studies in the human SC and amygdala (Almeida et al, 2013(Almeida et al, , 2015, suggest that faces are also associated with central-biased representation in the subcortical visual system.…”

Amygdala Response to Emotional Stimuli without Awareness: Facts and Interpretations

“…Visual stimuli associated to danger in our evolutionary past, such as snakes and spiders, have also been studied during attentional and sensory unawareness. Non-conscious exposure to these stimuli evokes physiological arousal and amygdala response (Carlsson et al, 2004; Wendt et al, 2008; Alpers et al, 2009; Almeida et al, 2015), particularly if participants were phobic to these classes of stimuli, and activated Amg also when unattended because presented in the affected side of patients with hemispatial neglect (Tamietto et al, 2015). On the other hand, the alleged special status of faces in triggering non-conscious perception and Amg activity is at odd with negative evidence when non-emotional facial characteristics, such as gender or identity, are tested during unawareness (Rossion et al, 2000; Negro et al, 2015).…”

A Rapid Subcortical Amygdala Route for Faces Irrespective of Spatial Frequency and Emotion

“…This is supported by the latency of the emotion effects we observed at the sensor level (occurring at approximately 150ms). Some degree of pre-emptive processing in the pulvinar, however, is supported by previous research on pulvinar response-specificity to faces 24,56 and snakes 24,57,58 . There has been debate, though, over whether these pulvinar responses are generated independently or are a result of cortical mediation 6,8 .…”