TMS disruption of the lateral prefrontal cortex increases neural activity in the default mode network when naming facial expressions.

Recognizing facial expressions is dependent on multiple brain networks specialized for different cognitive functions. In the current study, participants (N = 20) were scanned using functional magnetic resonance imaging (fMRI), while they performed a covert facial expression naming task. Immediately prior to scanning thetaburst transcranial magnetic stimulation (TMS) was delivered over the right lateral prefrontal cortex (PFC), or the vertex control site. A group whole-brain analysis revealed that TMS induced opposite effects in the neural responses across different brain networks. Stimulation of the right PFC (compared to stimulation of the vertex) decreased neural activity in the left lateral PFC but increased neural activity in three nodes of the default mode network (DMN): the right superior frontal gyrus, right angular gyrus and the bilateral middle cingulate gyrus. A region of interest analysis showed that TMS delivered over the right PFC reduced neural activity across all functionally localised face areas (including in the PFC) compared to TMS delivered over the vertex. These results suggest that visually recognizing facial expressions is dependent on the dynamic interaction of the face-processing network and the DMN. Our study also demonstrates the utility of combined TMS/fMRI studies for revealing the dynamic interactions between different functional brain networks.

Distinct patterns of neural response to faces from different races in humans and deep networks.

Social categories such as the race or ethnicity of an individual are typically conveyed by the visual appearance of the face. The aim of this study was to explore how these differences in facial appearance are represented in human and artificial neural networks. First, we compared the similarity of faces from different races using a neural network trained to discriminate identity. We found that the differences between races were most evident in the fully connected layers of the network. Although these layers were also able to predict behavioural judgements of face identity from human participants, performance was biased toward White faces. Next, we measured the neural response in face-selective regions of the human brain to faces from different races in Asian and White participants. We found distinct patterns of response to faces from different races in face-selective regions. We also found that the spatial pattern of response was more consistent across participants for own-race compared to other-race faces. Together, these findings show that faces from different races elicit different patterns of response in human and artificial neural networks. These differences may underlie the ability to make categorical judgements and explain the behavioural advantage for the recognition of own-race faces.

Measuring the response to visually presented faces in the human lateral prefrontal cortex.

Neuroimaging studies identify multiple face-selective areas in the human brain. In the current study, we compared the functional response of the face area in the lateral prefrontal cortex to that of other face-selective areas. In Experiment 1, participants (n = 32) were scanned viewing videos containing faces, bodies, scenes, objects, and scrambled objects. We identified a face-selective area in the right inferior frontal gyrus (rIFG). In Experiment 2, participants (n = 24) viewed the same videos or static images. Results showed that the rIFG, right posterior superior temporal sulcus (rpSTS), and right occipital face area (rOFA) exhibited a greater response to moving than static faces. In Experiment 3, participants (n = 18) viewed face videos in the contralateral and ipsilateral visual fields. Results showed that the rIFG and rpSTS showed no visual field bias, while the rOFA and right fusiform face area (rFFA) showed a contralateral bias. These experiments suggest two conclusions; firstly, in all three experiments, the face area in the IFG was not as reliably identified as face areas in the occipitotemporal cortex. Secondly, the similarity of the response profiles in the IFG and pSTS suggests the areas may perform similar cognitive functions, a conclusion consistent with prior neuroanatomical and functional connectivity evidence.

Face learning via brief real-world social interactions induces changes in face-selective brain areas and hippocampus.

Making new acquaintances requires learning to recognise previously unfamiliar faces. In the current study, we investigated this process by staging real-world social interactions between actors and the participants. Participants completed a face-matching behavioural task in which they matched photographs of the actors (whom they had yet to meet), or faces similar to the actors (henceforth called foils). Participants were then scanned using functional magnetic resonance imaging (fMRI) while viewing photographs of actors and foils. Immediately after exiting the scanner, participants met the actors for the first time and interacted with them for 10 min. On subsequent days, participants completed a second behavioural experiment and then a second fMRI scan. Prior to each session, actors again interacted with the participants for 10 min. Behavioural results showed that social interactions improved performance accuracy when matching actor photographs, but not foil photographs. The fMRI analysis revealed a difference in the neural response to actor photographs and foil photographs across all regions of interest (ROIs) only after social interactions had occurred. Our results demonstrate that short social interactions were sufficient to learn and discriminate previously unfamiliar individuals. Moreover, these learning effects were present in brain areas involved in face processing and memory.

Stimulating parietal regions of the multiple-demand cortex impairs novel vocabulary learning.

Neuroimaging research demonstrated that the early stages of learning engage domain-general networks, non-specialist brain regions that process a wide variety of cognitive tasks. Those networks gradually disengage as learning progresses and learned information becomes processed in brain networks specialised for the specific function (e.g., language). In the current study, we used repetitive transcranial magnetic stimulation (rTMS) in the form of continuous theta burst stimulation (cTBS) to test whether stimulation of the bilateral parietal region of the domain-general network impairs learning new vocabulary, indicating its causal engagement in this process. Twenty participants, with no prior knowledge of Polish, learned Polish words for well-known objects across three training stages. The first training stage started with cTBS applied to either the experimental domain-general bilateral parietal site or the control bilateral precentral site. Immediately after cTBS, the vocabulary training commenced. A different set of words was learned for each site. Immediately after the training stage, participants performed a novel vocabulary test, designed to measure their knowledge of the new words and the effect of stimulation on learning. To measure stimulation effect when the words were more established in the mental lexicon, participants received additional training on the same words but without cTBS (second training stage) and then the full procedures from the first training stage were repeated (third training stage). Results demonstrated that stimulation impaired novel word learning when applied to the bilateral parietal site at the first stage of learning only. This effect was not present when newly learned words were used more proficiently in the third training stage, or at any learning stage during control site stimulation. Our results show that the bilateral parietal region of the domain-general network causally contributes to the successful learning of novel words.

Dissociable pathways for moving and static face perception begin in early visual cortex: Evidence from an acquired prosopagnosic.

To investigate the functional connections between the core components of the face processing network we tested Herschel, an acquired prosopagnosic patient with a right ventral occipitotemporal lesion. In Experiment 1, Herschel, and control participants, were scanned with functional magnetic resonance imaging (fMRI) while viewing videos of moving faces, or static images taken from the videos. In Experiment 2, participants viewed videos of actors making facial expressions, or static images taken from the videos. In Experiment 3, participants viewed videos of moving faces presented in the left or right visual field. Results showed the neural response in Herschel's right occipital face area (OFA) was impaired for moving and static faces (Experiment 1), moving expressions (Experiment 2) and moving faces in the left visual field (Experiment 3). The response in Herschel's right fusiform face area (FFA) to moving and static faces was impaired in Experiment 1 only, in Experiments 2 and 3 Herschel's FFA response was not significantly different from controls. By contrast, the response in Herschel's right posterior superior temporal sulcus (rpSTS) to moving and static faces and expressions (Experiments 1 and 2) and the visual field response (Experiment 3) was not significantly different from control participants. Our results demonstrate there are cortico-cortical inputs to the pSTS from early visual cortex that are independent of the OFA, a conclusion inconsistent with established models of face processing.

Dual-site TMS demonstrates causal functional connectivity between the left and right posterior temporal sulci during facial expression recognition.

BACKGROUND: Neuroimaging studies suggest that facial expression recognition is processed in the bilateral posterior superior temporal sulcus (pSTS). Our recent repetitive transcranial magnetic stimulation (rTMS) study demonstrates that the bilateral pSTS is causally involved in expression recognition, although involvement of the right pSTS is greater than involvement of the left pSTS. OBJECTIVE: /Hypothesis: In this study, we used a dual-site TMS to investigate whether the left pSTS is functionally connected to the right pSTS during expression recognition. We predicted that if this connection exists, simultaneous TMS disruption of the bilateral pSTS would impair expression recognition to a greater extent than unilateral stimulation of the right pSTS alone. METHODS: Participants attended two TMS sessions. In Session 1, participants performed an expression recognition task while rTMS was delivered to the face-sensitive right pSTS (experimental site), object-sensitive right lateral occipital complex (control site) or no rTMS was delivered (behavioural control). In Session 2, the same experimental design was used, except that continuous theta-burst stimulation (cTBS) was delivered to the left pSTS immediately before behavioural testing commenced. Session order was counter-balanced across participants. RESULTS: In Session 1, rTMS to the rpSTS impaired performance accuracy compared to the control conditions. Crucially in Session 2, the size of this impairment effect doubled after cTBS was delivered to the left pSTS. CONCLUSIONS: Our results provide evidence for a causal functional connection between the left and right pSTS during expression recognition. In addition, this study further demonstrates the utility of the dual-site TMS for investigating causal functional links between brain regions.

Functional hierarchy for tactile processing in the visual cortex of sighted adults.

Perception via different sensory modalities was traditionally believed to be supported by largely separate brain systems. However, a growing number of studies demonstrate that the visual cortices of typical, sighted adults are involved in tactile and auditory perceptual processing. Here, we investigated the spatiotemporal dynamics of the visual cortex's involvement in a complex tactile task: Braille letter recognition. Sighted subjects underwent Braille training and then participated in a transcranial magnetic stimulation (TMS) study in which they tactually identified single Braille letters. During this task, TMS was applied to their left early visual cortex, visual word form area (VWFA), and left early somatosensory cortex at five time windows from 20 to 520 ms following the Braille letter presentation's onset. The subjects' response accuracy decreased when TMS was applied to the early visual cortex at the 120-220 ms time window and when TMS was applied to the VWFA at the 320-420 ms time window. Stimulation of the early somatosensory cortex did not have a time-specific effect on the accuracy of the subjects' Braille letter recognition, but rather caused a general slowdown during this task. Our results indicate that the involvement of sighted people's visual cortices in tactile perception respects the canonical visual hierarchy-the early tactile processing stages involve the early visual cortex, whereas more advanced tactile computations involve high-level visual areas. Our findings are compatible with the metamodal account of brain organization and suggest that the whole visual cortex may potentially support spatial perception in a task-specific, sensory-independent manner.

TMS demonstrates that both right and left superior temporal sulci are important for facial expression recognition.

Prior studies demonstrate that a face-responsive region in the posterior superior temporal sulcus (pSTS) is involved in facial expression recognition. Although this region can be identified in both hemispheres, studies more commonly report it in the right hemisphere. However, the extent to which expression recognition is lateralised in pSTS remains unclear. In the current study, we used transcranial magnetic stimulation (TMS) to systematically compare the causal contribution of the right pSTS (rpSTS) with the left pSTS (lpSTS) during facial expression recognition. TMS was delivered over the functionally localised rpSTS, lpSTS and the control vertex site while participants (N = 30) performed an expression matching task and a control object matching task. TMS delivered over the rpSTS impaired expression recognition more than TMS delivered over the lpSTS. Crucially, TMS delivered over the rpSTS and lpSTS impaired task performance more than TMS delivered over the control site. TMS had no effect on the control task. This causally demonstrates that while task disruption was greater in the rpSTS, both the rpSTS and the lpSTS were engaged in facial expression recognition. Our results indicate that cognitive functions that are seemingly lateralised in neuroimaging studies, still rely on computations performed in both hemispheres for optimum task performance.

Stimulating Multiple-Demand Cortex Enhances Vocabulary Learning.

It is well established that networks within multiple-demand cortex (MDC) become active when diverse skills and behaviors are being learnt. However, their causal role in learning remains to be established. In the present study, we first performed functional magnetic resonance imaging on healthy female and male human participants to confirm that MDC was most active in the initial stages of learning a novel vocabulary, consisting of pronounceable nonwords (pseudowords), each associated with a picture of a real object. We then examined, in healthy female and male human participants, whether repetitive transcranial magnetic stimulation of a frontal midline node of the cingulo-opercular MDC affected learning rates specifically during the initial stages of learning. We report that stimulation of this node, but not a control brain region, substantially improved both accuracy and response times during the earliest stage of learning pseudoword-object associations. This stimulation had no effect on the processing of established vocabulary, tested by the accuracy and response times when participants decided whether a real word was accurately paired with a picture of an object. These results provide evidence that noninvasive stimulation to MDC nodes can enhance learning rates, thereby demonstrating their causal role in the learning process. We propose that this causal role makes MDC candidate target for experimental therapeutics; for example, in stroke patients with aphasia attempting to reacquire a vocabulary.SIGNIFICANCE STATEMENT Learning a task involves the brain system within which that specific task becomes established. Therefore, successfully learning a new vocabulary establishes the novel words in the language system. However, there is evidence that in the early stages of learning, networks within multiple-demand cortex (MDC), which control higher cognitive functions, such as working memory, attention, and monitoring of performance, become active. This activity declines once the task is learnt. The present study demonstrated that a node within MDC, located in midline frontal cortex, becomes active during the early stage of learning a novel vocabulary. Importantly, noninvasive brain stimulation of this node improved performance during this stage of learning. This observation demonstrated that MDC activity is important for learning.

Massive cortical reorganization in sighted Braille readers.

The brain is capable of large-scale reorganization in blindness or after massive injury. Such reorganization crosses the division into separate sensory cortices (visual, somatosensory...). As its result, the visual cortex of the blind becomes active during tactile Braille reading. Although the possibility of such reorganization in the normal, adult brain has been raised, definitive evidence has been lacking. Here, we demonstrate such extensive reorganization in normal, sighted adults who learned Braille while their brain activity was investigated with fMRI and transcranial magnetic stimulation (TMS). Subjects showed enhanced activity for tactile reading in the visual cortex, including the visual word form area (VWFA) that was modulated by their Braille reading speed and strengthened resting-state connectivity between visual and somatosensory cortices. Moreover, TMS disruption of VWFA activity decreased their tactile reading accuracy. Our results indicate that large-scale reorganization is a viable mechanism recruited when learning complex skills.

Inferior parietal lobule contributions to visual word recognition.

This study investigated how the left inferior parietal lobule (IPL) contributes to visual word recognition. We used repetitive TMS to temporarily disrupt neural information processing in two anatomical fields of the IPL, namely, the angular (ANG) and supramarginal (SMG) gyri, and observed the effects on reading tasks that focused attention on either the meaning or sounds of written words. Relative to no TMS, stimulation of the left ANG selectively slowed responses in the meaning, but not sound, task, whereas stimulation of the left SMG affected responses in the sound, but not meaning, task. These results demonstrate that ANG and SMG doubly dissociate in their contributions to visual word recognition. We suggest that this functional division of labor may be understood in terms of the distinct patterns of cortico-cortical connectivity resulting in separable functional circuits.

Transcranial magnetic stimulation for investigating causal brain-behavioral relationships and their time course.

Transcranial magnetic stimulation (TMS) is a safe, non-invasive brain stimulation technique that uses a strong electromagnet in order to temporarily disrupt information processing in a brain region, generating a short-lived "virtual lesion." Stimulation that interferes with task performance indicates that the affected brain region is necessary to perform the task normally. In other words, unlike neuroimaging methods such as functional magnetic resonance imaging (fMRI) that indicate correlations between brain and behavior, TMS can be used to demonstrate causal brain-behavior relations. Furthermore, by varying the duration and onset of the virtual lesion, TMS can also reveal the time course of normal processing. As a result, TMS has become an important tool in cognitive neuroscience. Advantages of the technique over lesion-deficit studies include better spatial-temporal precision of the disruption effect, the ability to use participants as their own control subjects, and the accessibility of participants. Limitations include concurrent auditory and somatosensory stimulation that may influence task performance, limited access to structures more than a few centimeters from the surface of the scalp, and the relatively large space of free parameters that need to be optimized in order for the experiment to work. Experimental designs that give careful consideration to appropriate control conditions help to address these concerns. This article illustrates these issues with TMS results that investigate the spatial and temporal contributions of the left supramarginal gyrus (SMG) to reading.

Early and sustained supramarginal gyrus contributions to phonological processing.

Reading is a difficult task that, at a minimum, requires recognizing a visual stimulus and linking it with its corresponding sound and meaning. Neurologically, this involves an anatomically distributed set of brain regions cooperating to solve the problem. It has been hypothesized that the supramarginal gyrus (SMG) contributes preferentially to phonological aspects of word processing and thus plays an important role in visual word recognition. Here, we used chronometric transcranial magnetic stimulation (TMS) to investigate the functional specificity and timing of SMG involvement in reading visually presented words. Participants performed tasks designed to focus on either the phonological, semantic, or visual aspects of written words while double pulses of TMS (delivered 40 ms apart) were used to temporarily interfere with neural information processing in the left SMG at five different time windows. Stimulation at 80/120, 120/160, and 160/200 ms post-stimulus onset significantly slowed subjects' reaction times in the phonological task. This inhibitory effect was specific to the phonological condition, with no effect of TMS in the semantic or visual tasks, consistent with claims that SMG contributes preferentially to phonological aspects of word processing. The fact that the effect began within 80-120 ms of the onset of the stimulus and continued for approximately 100 ms, indicates that phonological processing initiates early and is sustained over time. These findings are consistent with accounts of visual word recognition that posit parallel activation of orthographic, phonological, and semantic information that interact over time to settle into a distributed, but stable, representation of a word.