The influence of subcortical shortcuts on disordered sensory and cognitive processing.

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.

Neural and computational processes of accelerated perceptual awareness and decisions: A 7T fMRI study.

Rapidly detecting salient information in our environments is critical for survival. Visual processing in subcortical areas like the pulvinar and amygdala has been shown to facilitate unconscious processing of salient stimuli. It is unknown, however, if and how these areas might interact with cortical regions to facilitate faster conscious perception of salient stimuli. Here we investigated these neural processes using 7T functional magnetic resonance imaging (fMRI) in concert with computational modelling while participants (n = 33) engaged in a breaking continuous flash suppression paradigm (bCFS) in which fearful and neutral faces are initially suppressed from conscious perception but then eventually 'breakthrough' into awareness. Participants reported faster breakthrough times for fearful faces compared with neutral faces. Drift-diffusion modelling suggested that perceptual evidence was accumulated at a faster rate for fearful faces compared with neutral faces. For both neutral and fearful faces, faster response times were associated with greater activity in the amygdala (specifically within its subregions, including superficial, basolateral and amygdalo-striatal transition area) and the insula. Faster rates of evidence accumulation coincided with greater activity in frontoparietal regions and occipital lobe, as well as the amygdala. A lower decision-boundary correlated with activity in the insula and the posterior cingulate cortex (PCC), but not with the amygdala. Overall, our findings suggest that hastened perceptual awareness of salient stimuli recruits the amygdala and, more specifically, is driven by accelerated evidence accumulation in fronto-parietal and visual areas. In sum, we have mapped distinct neural computations that accelerate perceptual awareness of visually suppressed faces.

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

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."SIGNIFICANCE STATEMENT The human amygdala coordinates how we respond to biologically relevant stimuli, such as threat or reward. It has been postulated that the amygdala first receives visual input via a rapid subcortical route that conveys "coarse" information, namely, low spatial frequencies. For the first time, the present paper provides direction-specific evidence from computational modeling that the subcortical route plays a generalized role in visual processing by rapidly transmitting raw, unfiltered information directly to the amygdala. This calls into question a widely held assumption across human and animal research that fear responses are produced faster by low spatial frequencies. Our proposed mechanism suggests organisms quickly generate fear responses to a wide range of visual properties, heavily implicating future research on anxiety-prevention strategies.

Implicit agency in observed actions: evidence for N1 suppression of tones caused by self-made and observed actions.

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 others' 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 others' 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 others' 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.

Spatiotemporal Precision of Neuroimaging in Psychiatry.

Aberrant patterns of cognition, perception, and behavior seen in psychiatric disorders are thought to be driven by a complex interplay of neural processes that evolve at a rapid temporal scale. Understanding these dynamic processes in vivo in humans has been hampered by a trade-off between spatial and temporal resolutions inherent to current neuroimaging technology. A recent trend in psychiatric research has been the use of high temporal resolution imaging, particularly magnetoencephalography, often in conjunction with sophisticated machine learning decoding techniques. Developments here promise novel insights into the spatiotemporal dynamics of cognitive phenomena, including domains relevant to psychiatric illnesses such as reward and avoidance learning, memory, and planning. This review considers recent advances afforded by exploiting this increased spatiotemporal precision, with specific reference to applications that seek to drive a mechanistic understanding of psychopathology and the realization of preclinical translation.

Differential replay of reward and punishment paths predicts approach and avoidance.

Neural replay is implicated in planning, where states relevant to a task goal are rapidly reactivated in sequence. It remains unclear whether, during planning, replay relates to an actual prospective choice. Here, using magnetoencephalography (MEG), we studied replay in human participants while they planned to either approach or avoid an uncertain environment containing paths leading to reward or punishment. We find evidence for forward sequential replay during planning, with rapid state-to-state transitions from 20 to 90 ms. Replay of rewarding paths was boosted, relative to aversive paths, before a decision to avoid and attenuated before a decision to approach. A trial-by-trial bias toward replaying prospective punishing paths predicted irrational decisions to approach riskier environments, an effect more pronounced in participants with higher trait anxiety. The findings indicate a coupling of replay with planned behavior, where replay prioritizes an online representation of a worst-case scenario for approaching or avoiding.

Surprising Threats Accelerate Conscious Perception.

The folk psychological notion that "we see what we expect to see" is supported by evidence that we become consciously aware of visual stimuli that match our prior expectations more quickly than stimuli that violate our expectations. Similarly, "we see what we want to see," such that more biologically-relevant stimuli are also prioritised for conscious perception. How, then, is perception shaped by biologically-relevant stimuli that we did not expect? Here, we conducted two experiments using breaking continuous flash suppression (bCFS) to investigate how prior expectations modulated response times to neutral and fearful faces. In both experiments, we found that prior expectations for neutral faces hastened responses, whereas the opposite was true for fearful faces. This interaction between emotional expression and prior expectations was driven predominantly by participants with higher trait anxiety. Electroencephalography (EEG) data collected in Experiment 2 revealed an interaction evident in the earliest stages of sensory encoding, suggesting prediction errors expedite sensory encoding of fearful faces. These findings support a survival hypothesis, where biologically-relevant fearful stimuli are prioritised for conscious access even more so when unexpected, especially for people with high trait anxiety.

Doorways do not always cause forgetting: a multimodal investigation.

BACKGROUND: The 'doorway effect', or 'location updating effect', claims that we tend to forget items of recent significance immediately after crossing a boundary. Previous research suggests that such a forgetting effect occurs both at physical boundaries (e.g., moving from one room to another via a door) and metaphysical boundaries (e.g., imagining traversing a doorway, or even when moving from one desktop window to another on a computer). Here, we aimed to conceptually replicate this effect using virtual and physical environments. METHODS: Across four experiments, we measured participants' hit and false alarm rates to memory probes for items recently encountered either in the same or previous room. Experiments 1 and 2 used highly immersive virtual reality without and with working memory load (Experiments 1 and 2, respectively). Experiment 3 used passive video watching and Experiment 4 used active real-life movement. Data analysis was conducted using frequentist as well as Bayesian inference statistics. RESULTS: Across this series of experiments, we observed no significant effect of doorways on forgetting. In Experiment 2, however, signal detection was impaired when participants responded to probes after moving through doorways, such that false alarm rates were increased for mismatched recognition probes. Thus, under working memory load, memory was more susceptible to interference after moving through doorways. CONCLUSIONS: This study presents evidence that is inconsistent with the location updating effect as it has previously been reported. Our findings call into question the generalisability and robustness of this effect to slight paradigm alterations and, indeed, what factors contributed to the effect observed in previous studies.

Behavioral and Neural Effects of Familiarization on Object-Background Associations.

Associative memory is the ability to link together components of stimuli. Previous evidence suggests that prior familiarization with study items affects the nature of the association between stimuli. More specifically, novel stimuli are learned in a more context-dependent fashion than stimuli that have been encountered previously without the current context. In the current study, we first acquired behavioral data from 62 human participants to conceptually replicate this effect. Participants were instructed to memorize multiple object-scene pairs (study phase) and were then tested on their recognition memory for the objects (test phase). Importantly, 1 day prior, participants had been familiarized with half of the object stimuli. During the test phase, the objects were either matched to the same scene as during study (intact pair) or swapped with a different object's scene (rearranged pair). Our results conceptually replicated the context-dependency effect by showing that breaking up a studied object-context pairing is more detrimental to object recognition performance for non-familiarized objects than for familiarized objects. Second, we used functional magnetic resonance imaging (fMRI) to determine whether medial temporal lobe encoding-related activity patterns are reflective of this familiarity-related context effect. Data acquired from 25 human participants indicated a larger effect of familiarization on encoding-related hippocampal activity for objects presented within a scene context compared to objects presented alone. Our results showed that both retrieval-related accuracy patterns and hippocampal activation patterns were in line with a familiarization-mediated context-dependency effect.

Investigating the Subcortical Route to the Amygdala Across Species and in Disordered Fear Responses.

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.

Survival of the Fittest: Increased Stimulus Competition During Encoding Results in Fewer but More Robust Memory Traces.

Forgetting can be accounted for by time-indexed decay as well as competition-based interference processes. Although conventionally seen as competing theories of forgetting processes, Altmann and colleagues argued for a functional interaction between decay and interference. They revealed that, in short-term memory, time-based forgetting occurred at a faster rate under conditions of high proactive interference compared to conditions of low proactive interference. However, it is unknown whether interactive effects between decay-based forgetting and interference-based forgetting also exist in long-term memory. We employed a delayed memory recognition paradigm for visual indoor and outdoor scenes, measuring recognition accuracy at two time-points, immediately after learning and after 1 week, while interference was indexed by the number of images in a semantic category. We found that higher levels of interference during encoding led to a slower subsequent decay rate. In contrast to the findings in working-memory, our results suggest that a "survival of the fittest" principle applies to long-term memory processes, in which stimulus competition during encoding results in fewer, but also more robust memory traces, which decay at a slower rate. Conversely, low levels of interference during encoding allow more memory traces to form initially, which, however, subsequently decay at a faster rate. Our findings provide new insights into the mechanism of forgetting and could inform neurobiological models of forgetting.

An afferent white matter pathway from the pulvinar to the amygdala facilitates fear recognition.

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).

Neural Correlates of Temporal Complexity and Synchrony during Audiovisual Correspondence Detection.

We often perceive real-life objects as multisensory cues through space and time. A key challenge for audiovisual integration is to match neural signals that not only originate from different sensory modalities but also that typically reach the observer at slightly different times. In humans, complex, unpredictable audiovisual streams lead to higher levels of perceptual coherence than predictable, rhythmic streams. In addition, perceptual coherence for complex signals seems less affected by increased asynchrony between visual and auditory modalities than for simple signals. Here, we used functional magnetic resonance imaging to determine the human neural correlates of audiovisual signals with different levels of temporal complexity and synchrony. Our study demonstrated that greater perceptual asynchrony and lower signal complexity impaired performance in an audiovisual coherence-matching task. Differences in asynchrony and complexity were also underpinned by a partially different set of brain regions. In particular, our results suggest that, while regions in the dorsolateral prefrontal cortex (DLPFC) were modulated by differences in memory load due to stimulus asynchrony, areas traditionally thought to be involved in speech production and recognition, such as the inferior frontal and superior temporal cortex, were modulated by the temporal complexity of the audiovisual signals. Our results, therefore, indicate specific processing roles for different subregions of the fronto-temporal cortex during audiovisual coherence detection.

Right wing authoritarianism is associated with race bias in face detection.

Racial discrimination can be observed in a wide range of psychological processes, including even the earliest phases of face detection. It remains unclear, however, whether racially-biased low-level face processing is influenced by ideologies, such as right wing authoritarianism or social dominance orientation. In the current study, we hypothesized that socio-political ideologies such as these can substantially predict perceptive racial bias during early perception. To test this hypothesis, 67 participants detected faces within arrays of neutral objects. The faces were either Caucasian (in-group) or North African (out-group) and either had a neutral or angry expression. Results showed that participants with higher self-reported right-wing authoritarianism were more likely to show slower response times for detecting out- vs. in-groups faces. We interpreted our results according to the Dual Process Motivational Model and suggest that socio-political ideologies may foster early racial bias via attentional disengagement.

Racial bias in neural response to others' pain is reduced with other-race contact.

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.