There is significant controversy over the existence and function of a direct subcortical visual pathway to the amygdala. It is thought that this pathway rapidly transmits low spatial frequency information to the amygdala independently of the cortex, and yet the directionality of this function has never been determined. We used magnetoencephalography to measure neural activity while human participants discriminated the gender of neutral and fearful faces filtered for low or high spatial frequencies. We applied dynamic causal modeling to demonstrate that the most likely underlying neural network consisted of a pulvinar-amygdala connection that was uninfluenced by spatial frequency or emotion, and a cortical-amygdala connection that conveyed high spatial frequencies. Crucially, data-driven neural simulations revealed a clear temporal advantage of the subcortical connection over the cortical connection in influencing amygdala activity. Thus, our findings support the existence of a rapid subcortical pathway that is nonselective in terms of the spatial frequency or emotional content of faces. We propose that that the "coarseness" of the subcortical route may be better reframed as "generalized."

Our ability to rapidly detect threats is thought to be subserved by a subcortical pathway that quickly conveys visual information to the amygdala. This neural shortcut has been demonstrated in animals but has rarely been shown in the human brain. Importantly, it remains unclear whether such a pathway might influence neural activity and behavior. We conducted a multimodal neuroimaging study of 622 participants from the Human Connectome Project. We applied probabilistic tractography to diffusion-weighted images, reconstructing a subcortical pathway to the amygdala from the superior colliculus via the pulvinar. We then computationally modeled the flow of haemodynamic activity during a face-viewing task and found evidence for a functionally afferent pulvinar-amygdala pathway. Critically, individuals with greater fibre density in this pathway also had stronger dynamic coupling and enhanced fearful face recognition. Our findings provide converging evidence for the recruitment of an afferent subcortical pulvinar connection to the amygdala that facilitates fear recognition.Editorial note: This article has been through an editorial process in which the authors decide how to respond to the issues raised during peer review. The Reviewing Editor's assessment is that minor issues remain unresolved (see decision letter).

The very earliest stages of sensory processing have the potential to alter how we perceive and respond to our environment. These initial processing circuits can incorporate subcortical regions, such as the thalamus and brainstem nuclei, which mediate complex interactions with the brain's cortical processing hierarchy. These subcortical pathways, many of which we share with other animals, are not merely vestigial but appear to function as 'shortcuts' that ensure processing efficiency and preservation of vital life-preserving functions, such as harm avoidance, adaptive social interactions and efficient decision-making. Here, we propose that functional interactions between these higher-order and lower-order brain areas contribute to atypical sensory and cognitive processing that characterizes numerous neuropsychiatric disorders.

Observing the pain of others has been shown to elicit greater activation in sensory and emotional areas of the brain suggested to represent a neural marker of empathy. This modulation of brain responses to others' pain is dependent on the race of the observed person, such that observing own-race people in pain is associated with greater activity in the anterior cingulate and bilateral insula cortices compared to other-race people. Importantly, it is not known how this racial bias to pain in other-race individuals might change over time in new immigrants or might depend on the level and quality of contact with people of the other-race. We investigated these issues by recruiting Chinese students who had first arrived in Australia within the past 6 months to 5 years and assessing their level of contact with other races across different social contexts using comprehensive rating scales. During fMRI, participants observed videos of own-race/other-race individuals, as well as own-group/other-group individuals, receiving painful or non-painful touch. The typical racial bias in neural responses to observed pain was evident, whereby activation in the anterior cingulate cortex (ACC) was greater for pain in own-race compared to other-race people. Crucially, activation in the anterior cingulate to pain in other races increased significantly with the level of contact participants reported with people of the other race. Importantly, this correlation did not depend on the closeness of contact or personal relationships, but simply on the overall level of experience with people of the other race in their every-day environment. Racial bias in neural responses to others' pain, as a neural marker of empathy, therefore changes with experience in new immigrants at least within 5 years of arrival in the new society and, crucially, depends on the level of contact with people of the other race in every-day life contexts.

Abstract■ Every day we make attributions about how our actions and the actions of others cause consequences in the world around us. It is unknown whether we use the same implicit process in attributing causality when observing othersʼ actions as we do when making our own. The aim of this research was to investigate the neural processes involved in the implicit sense of agency we form between actions and effects, for both our own actions and when watching othersʼ actions. Using an interval estimation paradigm to elicit intentional binding in self-made and observed actions, we measured the EEG responses indicative of anticipatory processes before an action and the ERPs in response to the sensory consequence. We replicated our previous findings that we form a sense of implicit agency over our own and othersʼ actions. Crucially, EEG results showed that tones caused by either self-made or observed actions both resulted in suppression of the N1 component of the sensory ERP, with no difference in suppression between consequences caused by observed actions compared with self-made actions. Furthermore, this N1 suppression was greatest for tones caused by observed goal-directed actions rather than non-action or non-goal-related visual events. This suggests that top-down processes act upon the neural responses to sensory events caused by goal-directed actions in the same way for events caused by the self or those made by other agents. ■

Over the past few decades, evidence has come to light that there is a rapid subcortical shortcut that transmits visual information to the amygdala, effectively bypassing the visual cortex. This pathway purportedly runs from the superior colliculus to the amygdala via the pulvinar, and thus presents a methodological challenge to study noninvasively in the human brain. Here, we present our recent work where we reliably reconstructed the white matter structure and directional flow of neural signal along this pathway in over 600 healthy young adults. Critically, we found structure-function relationships for the pulvinar-amygdala connection, where people with greater fibre density had stronger functional neural coupling and were also better at recognising fearful facial expressions. These results tie together recent anatomical evidence from other visual primates with very recent optogenetic research on rodents demonstrating a functional role of this pathway in producing fear responses. Here, we discuss how this pathway might operate alongside other thalamo-cortical circuits (such as pulvinar to middle temporal area) and how its structure and function may change according to the sensory input it receives. This newly established circuit might play a potentially important role in autism and/or anxiety disorders.

Our sense of agency is thought to arise from the predictive nature of the action system. While previous research supports the role of motor-specific identity prediction in the sense of agency, it remains unclear whether identity-specific predictions (e.g., the pitch of a tone) that are not uniquely associated with specific motor responses also have a significant role. In the present study, we recorded EEG activity during an interval estimation task to assess the impact of these identity-specific predictions on intentional binding, N1 suppression, and the P3b component. Intentional binding was found for all tones that followed self-made actions, regardless of identity-specific predictability of the tone (i.e., the probability of that specific tone following the action). For the N1 component, consequent tones that followed any preceding event, whether it was an action or initial control tone, resulted in N1 suppression; however, this N1 suppression was not significantly influenced by identity-specific predictions. In contrast, the P3b component was significantly influenced by identity-specific predictions, with a significantly larger P3b elicited by more unexpected tones (i.e., prediction-incongruent tones) than expected tones (i.e., prediction-congruent tones). The overall P3b response was also larger for tones following self-made actions. Based on these P3b findings, it appears that higher-cognitive processes are needed to track violations of identity-specific prediction when a single motor command elicits different sensory events. In conclusion, identity-specific predictions that are not associated with specific motor responses have a minimal impact on implicit measures of agency such as intentional binding and N1 suppression.

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