Using Live and Video Stimuli to Localize Face and Object Processing Regions of the Canine Brain

Previous research to localize face areas in dogs’ brains has generally relied on static images or videos. However, most dogs do not naturally engage with two-dimensional images, raising the question of whether dogs perceive such images as representations of real faces and objects. To measure the equivalency of live and two-dimensional stimuli in the dog’s brain, during functional magnetic resonance imaging (fMRI) we presented dogs and humans with live-action stimuli (actors and objects) as well as videos of the same actors and objects. The dogs (n = 7) and humans (n = 5) were presented with 20 s blocks of faces and objects in random order. In dogs, we found significant areas of increased activation in the putative dog face area, and in humans, we found significant areas of increased activation in the fusiform face area to both live and video stimuli. In both dogs and humans, we found areas of significant activation in the posterior superior temporal sulcus (ectosylvian fissure in dogs) and the lateral occipital complex (entolateral gyrus in dogs) to both live and video stimuli. Of these regions of interest, only the area along the ectosylvian fissure in dogs showed significantly more activation to live faces than to video faces, whereas, in humans, both the fusiform face area and posterior superior temporal sulcus responded significantly more to live conditions than video conditions. However, using the video conditions alone, we were able to localize all regions of interest in both dogs and humans. Therefore, videos can be used to localize these regions of interest, though live conditions may be more salient.

Using child-friendly movie stimuli to study the development of face, place, and object regions from age 3 to 12 years

Scanning young children while watching short, engaging, commercially-produced movies has emerged as a promising approach for increasing data retention and quality. Movie stimuli also evoke a richer variety of cognitive processes than traditional experiments - allowing the study of multiple aspects of brain development simultaneously. However, because these stimuli are uncontrolled, it is unclear how effectively distinct profiles of brain activity can be distinguished from the resulting data. Here we develop an approach for identifying multiple distinct subject-specific Regions of Interest (ssROIs) using fMRI data collected during movie-viewing. We focused on the test case of higher-level visual regions selective for faces, scenes, and objects. Adults (N=13) were scanned while viewing a 5.5 minute child-friendly movie, as well as a traditional experiment with isolated faces, scenes, and objects. We found that just 2.7 minutes of movie data could identify subject-specific face, scene, and object regions. While successful, the movie approach was still less effective than a traditional localizer. Having validated our approach in adults, we then used the same methods on movie data collected from 3-12-year-old children (N=122). Movie response timecourses in 3-year-old childrens face, scene, and object regions were already significantly and specifically predicted by timecourses from the corresponding regions in adults. We also found evidence of continued developmental change, particularly in the face-selective posterior superior temporal sulcus. Taken together, our results reveal both early maturity and functional change in face, scene, and object regions, and more broadly highlight the promise of short, child-friendly movies for developmental cognitive neuroscience.

Variability of neuronal responses in the posterior superior temporal sulcus predicts choice behavior during social interactions

Recent studies have shown that neural activity in a well-defined patch in the posterior superior temporal sulcus (the "gaze following patch", GFP) of the primate brain is strongly modulated when the other´s gaze attracts the observer's attention to locations/objects, the other is looking at. Changes of the mean discharge rate of neurons in the monkey GFP indicate that they are involved in two distinct computations: the allocation of spatial attention guided by the other´s gaze vector and the suppression of gaze following if inappropriate in a given situation. Here we asked if and how the discharge variability of neurons in the GFP is related to the task and, furthermore, if it carries information on behavioral performance. To this end, we calculated the Fano factor as a measure of across-trial discharge variability as a function of time. Our results show that all neurons exhibiting a task-related discharge-rate modulation also exhibit a stimulus onset-dependent drop in the Fano factor. Furthermore, the amplitude of the Fano factor reduction is modulated by task condition and the neuron's selectivity in this regard. We found that these effects are directly related to the monkeys' behavioral performance in that the Fano factor is predictive about upcoming correct or wrong decisions. Our results indicate that neuronal discharge variability as gauged by the Fano-factor, hitherto primarily studied in the context of visual perception or motor control, is an informative measure also in studies of the neural underpinnings of complex social behavior.

Effects of Aging on the Neural Mechanisms Underlying the Recollection of Memories Encoded by Social Interactions With Persons in the Same and Different Age Groups

Memories related to ingroup members are remembered more accurately than those related to outgroup members. However, little is known about the age-dependent differences in neural mechanisms underlying the retrieval of memories shared with ingroup or outgroup members that are categorized by age-group membership. The present functional magnetic resonance imaging (fMRI) study investigated this issue. Healthy young and older adults participated in a 2-day experiment. On the first day outside fMRI, participants were presented with words by unfamiliar persons in movie clips and exchanged each word with persons belonging to the same age group (SAG) or different age group (DAG). On the second day during fMRI, participants were randomly presented with learned and new words one by one, and they judged whether each word had been encoded with either SAG or DAG members or neither. fMRI results demonstrated that an age-dependent decrease in successful retrieval activation of memories presented by DAG was identified in the anterior temporal lobe (ATL) and hippocampus, whereas with memories presented by SAG, an age-dependent decrease in activation was not found in any regions. In addition, an age-dependent decrease in functional connectivity was significant between the hippocampus/ATL and posterior superior temporal sulcus (pSTS) during the successful retrieval of memories encoded with the DAG people. The “other”-related mechanisms including the hippocampus, ATL, and pSTS with memories learned with the outgroup members could decrease in older adults, whereas with memories learned with the ingroup members, the “self”-related mechanisms could be relatively preserved in older adults.

Investigating the influence of autism spectrum traits on face processing mechanisms in developmental prosopagnosia

Autism traits are commonly used as exclusionary criteria in studies of developmental prosopagnosia (DP). We investigated whether autism traits result in qualitatively different face processing in 43 DPs with high vs. low autism quotient (AQ) scores and 27 controls. Compared to controls, behavioral face recognition deficits were similar between the high and low AQ DP groups aside from worse emotion recognition in the high AQ DPs. Both DP groups showed reduced face selectivity in task-based fMRI, although higher AQ DPs showed decreased face selectivity in the posterior superior temporal sulcus. Resting-state fMRI showed similar face network connectivity between DP groups. This suggests that face processing is similar between the DP groups, with additional emotion processing deficits in higher AQ DPs.

Transcranial Magnetic Stimulation Over the Right Posterior Superior Temporal Sulcus Promotes the Feature Discrimination Processing

Attention is the dynamic process of allocating limited resources to the information that is most relevant to our goals. Accumulating studies have demonstrated the crucial role of frontal and parietal areas in attention. However, the effect of posterior superior temporal sulcus (pSTS) in attention is still unclear. To address this question, in this study, we measured transcranial magnetic stimulation (TMS)-induced event-related potentials (ERPs) to determine the extent of involvement of the right pSTS in attentional processing. We hypothesized that TMS would enhance the activation of the right pSTS during feature discrimination processing. We recruited 21 healthy subjects who performed the dual-feature delayed matching task while undergoing single-pulse sham or real TMS to the right pSTS 300 ms before the second stimulus onset. The results showed that the response time was reduced by real TMS of the pSTS as compared to sham stimulation. N270 amplitude was reduced during conflict processing, and the time-varying network analysis revealed increased connectivity between the frontal lobe and temporo-parietal and occipital regions. Thus, single-pulse TMS of the right pSTS enhances feature discrimination processing and task performance by reducing N270 amplitude and increasing connections between the frontal pole and temporo-parietal and occipital regions. These findings provide evidence that the right pSTS facilitates feature discrimination by accelerating the formation of a dynamic network.

Failure to engage the temporoparietal junction/posterior superior temporal sulcus predicts impaired naturalistic social cognition in schizophrenia

Schizophrenia is associated with marked impairments in social cognition. However, the neural correlates of these deficits remain unclear. Here we use naturalistic stimuli to examine the role of the right temporoparietal junction/posterior superior temporal sulcus (TPJ-pSTS)—an integrative hub for the cortical networks pertinent to the understanding complex social situations—in social inference, a key component of social cognition, in schizophrenia. 27 schizophrenia participants (SzP) and 21 healthy controls watched a clip of the movie “The Good, the Bad, and the Ugly” while high resolution multiband fMRI images were collected. We used inter-subject correlation (ISC) to measure the evoked activity, which we then compared to social cognition as measured by The Awareness of Social Inference Test (TASIT). We also compared between groups the TPJ-pSTS BOLD activity 1) relationship with the motion content in the movie, 2) synchronization with other cortical areas involved in the viewing of the movie, and 3) relationship with the frequency of saccades made during the movie. Activation deficits were greatest in middle TPJ (TPJm) and correlated significantly with impaired TASIT performance across groups. Follow-up analyses of the TPJ-pSTS revealed decreased synchronization with other cortical areas, decreased correlation with the motion content of the movie, and decreased correlation with the saccades made during the movie. The functional impairment of the TPJm, a hub area in the middle of the TPJ-pSTS, predicts deficits in social inference in SzP by disrupting the integration of visual motion processing into the TPJ. This disrupted integration then affects the use of the TPJ to guide saccades during the visual scanning of the movie clip. These findings suggest that the TPJ may be a treatment target for improving deficits in a key component of social cognition in SzP.

Top-Down Attention Guidance Shapes Action Encoding in the pSTS

The posterior superior temporal sulcus (pSTS) is a brain region characterized by perceptual representations of human body actions that promote the understanding of observed behavior. Increasingly, action observation is recognized as being strongly shaped by the expectations of the observer (Kilner 2011; Koster-Hale and Saxe 2013; Patel et al. 2019). Therefore, to characterize top-down influences on action observation, we evaluated the statistical structure of multivariate activation patterns from the action observation network (AON) while observers attended to the different dimensions of action vignettes (the action kinematics, goal, or identity of avatars jumping or crouching). Decoding accuracy varied as a function of attention instruction in the right pSTS and left inferior frontal cortex (IFC), with the right pSTS classifying actions most accurately when observers attended to the action kinematics and the left IFC classifying most accurately when observed attended to the actor’s goal. Functional connectivity also increased between the right pSTS and right IFC when observers attended to the actions portrayed in the vignettes. Our findings are evidence that the attentive state of the viewer modulates sensory representations in the pSTS, consistent with proposals that the pSTS occupies an interstitial zone mediating top-down context and bottom-up perceptual cues during action observation.

Intermittent theta burst stimulation over the posterior superior temporal sulcus for children with autism spectrum disorder: A 4-week randomized blinded controlled trial followed by another 4-week open-label intervention

The posterior superior temporal sulcus is a potential therapeutic target of brain stimulation for autism spectrum disorder. We conducted a 4-week randomized, single-blind parallel sham-controlled trial, followed by additional 4-week open-label intervention to evaluate the feasibility and efficacy regarding intermittent theta burst stimulation over the bilateral posterior superior temporal sulcus in autism spectrum disorder. In total, 78 intellectually able children and adolescents were randomized to the active ( n = 40) and sham groups ( n = 38). During the first 4 weeks, the active group received two-session/week intermittent theta burst stimulation, whereas the sham group received the same number of sham stimulation. After unblinding, both groups received eight-session real stimulation over the additional 4 weeks. In total, 91% participants completed the protocol with mild and transitory side-effects. There was no significant group-by-time interaction for active versus sham group on clinical symptoms and social cognitive performances in the first 4 weeks. The within-group analysis revealed 8 weeks (including a 4-week blind trial and a 4-week open-label intervention) of intermittent theta burst stimulation achieved greater efficacy than 4-week interventions. Participants with higher intelligence, better social cognitive performances, alongside less attention-deficit hyperactivity disorder severity at baseline, were more likely to be responders. Our study demonstrated the feasibility of long-term intermittent theta burst stimulation over the posterior superior temporal sulcus in children and adolescents with autism spectrum disorder. However, the findings from the first 4-week blind trial do not support the therapeutic efficacy of intermittent theta burst stimulation over the posterior superior temporal sulcus on the clinical symptoms and cognitive performance of social impairment, given the current stimulation protocol. The exploratory analyses suggest that the therapeutic efficacy might be moderated by several individual characteristics and more intermittent theta burst stimulation sessions. Lay abstract Intermittent theta burst stimulation is a varied form of repetitive transcranial magnetic non-invasive brain stimulation technique used to treat several neurological and psychiatric disorders. Its feasibility and therapeutic effects on the bilateral posterior superior temporal sulcus in children with autism are unknown. We conducted a single-blind, sham-controlled parallel randomized clinical trial in a hitherto largest sample of intellectually able children with autism ( N = 78). Participants randomized to the active group received two-session/week intermittent theta burst stimulation for continuous 8 weeks. Those in the sham group received two-session/week sham stimulations in the first 4 weeks and then active intervention for the following 4 weeks after unblinding. First, we found that continuous 8-week intermittent theta burst stimulation on the bilateral posterior superior temporal sulcus in children with autism is safe and tolerable. Second, we found that 8-week intermittent theta burst stimulation produced greater therapeutic efficacy, although we did not find any significant effects of 4-week intermittent theta burst stimulation on core symptoms and social cognitive performances in autism. Further analysis revealed that participants with higher intelligence and better social cognitive performance, alongside less attention-deficit hyperactivity disorder severity at baseline, were more likely to be responders. This study identified that the factors contribute to responders and the results suggest that longer courses of non-invasive brain stimulation may be needed to produce therapeutic benefits in autism, with consideration of heterogeneous responses.

Neuroimaging studies exploring the neural basis of social isolation

According to the social brain hypothesis, the human brain includes a network designed for the processing of social information. This network includes several brain regions that elaborate social cues, interactions and contexts, i.e. prefrontal paracingulate and parietal cortices, amygdala, temporal lobes and the posterior superior temporal sulcus. While current literature suggests the importance of this network from both a psychological and evolutionary perspective, little is known about its neurobiological bases. Specifically, only a paucity of studies explored the neural underpinnings of constructs that are ascribed to the social brain network functioning, i.e. objective social isolation and perceived loneliness. As such, this review aimed to overview neuroimaging studies that investigated social isolation in healthy subjects. Social isolation correlated with both structural and functional alterations within the social brain network and in other regions that seem to support mentalising and social processes (i.e. hippocampus, insula, ventral striatum and cerebellum). However, results are mixed possibly due to the heterogeneity of methods and study design. Future neuroimaging studies with longitudinal designs are needed to measure the effect of social isolation in experimental v. control groups and to explore its relationship with perceived loneliness, ultimately helping to clarify the neural correlates of the social brain.