Summary The causal role of an area within a neural network can be determined by interfering with its activity and measuring the impact. Many current reversible manipulation techniques have limitations preventing their application, particularly in deep areas of the primate brain. Here, we demonstrate that a focused transcranial ultrasound stimulation (TUS) protocol impacts activity even in deep brain areas: a subcortical brain structure, the amygdala (experiment 1), and a deep cortical region, the anterior cingulate cortex (ACC, experiment 2), in macaques. TUS neuromodulatory effects were measured by examining relationships between activity in each area and the rest of the brain using functional magnetic resonance imaging (fMRI). In control conditions without sonication, activity in a given area is related to activity in interconnected regions, but such relationships are reduced after sonication, specifically for the targeted areas. Dissociable and focal effects on neural activity could not be explained by auditory confounds.
When dealing with emotional situations, we often need to rapidly override automatic stimulus-response mappings and select an alternative course of action [1], for instance, when trying to manage, rather than avoid, another's aggressive behavior. The anterior prefrontal cortex (aPFC) has been linked to the control of these social emotional behaviors [2, 3]. We studied how this control is implemented by inhibiting the left aPFC with continuous theta burst stimulation (cTBS; [4]). The behavioral and cerebral consequences of this intervention were assessed with a task quantifying the control of social emotional actions and with concurrent measurements of brain perfusion. Inhibition of the aPFC led participants to commit more errors when they needed to select rule-driven responses overriding automatic action tendencies evoked by emotional faces. Concurrently, task-related perfusion decreased in bilateral aPFC and posterior parietal cortex and increased in amygdala and left fusiform face area. We infer that the aPFC controls social emotional behavior by upregulating regions involved in rule selection [5] and downregulating regions supporting the automatic evaluation of emotions [6]. These findings illustrate how exerting emotional control during social interactions requires the aPFC to coordinate rapid action selection processes, the detection of emotional conflicts, and the inhibition of emotionally-driven responses.
It is clear that the steroid hormone testosterone plays an important role in the regulation of social emotional behavior, but it remains unknown which neural circuits mediate these hormonal influences in humans. We investigated the modulatory effects of endogenous testosterone on the control of social emotional behavior by applying functional magnetic resonance imaging while healthy male participants performed a social approach–avoidance task. This task operationalized social emotional behavior by having participants approach and avoid emotional faces by pulling and pushing a joystick, respectively. Affect-congruent trials mapped the automatic tendency to approach happy faces and avoid angry faces. Affect-incongruent trials required participants to override those automatic action tendencies and select the opposite response (approach-angry, avoid-happy). The social emotional control required by affect-incongruent responses resulted in longer reaction times (RTs) and increased activity at the border of the ventrolateral prefrontal cortex and frontal pole (VLPFC/FP). We show that endogenous testosterone modulates these cerebral congruency effects through 2 mechanisms. First, participants with lower testosterone levels generate larger VLPFC/FP responses during affect-incongruent trials. Second, during the same trials, endogenous testosterone modulates the effective connectivity between the VLPFC/FP and the amygdala. These results indicate that endogenous testosterone influences local prefrontal activity and interregional connectivity supporting the control of social emotional behavior.
Grasping an object requires processing visuospatial information about the extrinsic features (spatial location) and intrinsic features (size, shape, orientation) of the object. Accordingly, manual prehension has been subdivided into a reach component, guiding the hand toward the object on the basis of its extrinsic features, and a grasp component, preshaping the fingers around the center of mass of the object on the basis of its intrinsic features. In neural terms, this distinction has been linked to a dedicated dorsomedial "reaching" circuit and a dorsolateral "grasping" circuit that process extrinsic and intrinsic features, linking occipital areas via parietal regions with the dorsal and ventral premotor cortex, respectively. We have tested an alternative possibility, namely that the relative contribution of the two circuits is related to the degree of on-line control required by the prehension movement.We used dynamic causal modeling of functional magnetic resonance imaging time series to assess how parieto-frontal connectivity is modulated by planning and executing prehension movements toward objects of different size and width. This experimental manipulation evoked different movements, with different planning and execution phases for the different objects. Crucially, grasping large objects increased inter-regional couplings within the dorsomedial circuit, whereas grasping small objects increased the effective connectivity of a mainly dorsolateral circuit, with a degree of overlap between these circuits. These results argue against the presence of dedicated cerebral circuits for reaching and grasping, suggesting that the contributions of the dorsolateral and the dorsomedial circuits are a function of the degree of on-line control required by the movement.
Comparing the brains of related species faces the challenges of establishing homologies whilst accommodating evolutionary specializations. Here we propose a general framework for understanding similarities and differences between the brains of primates. The approach uses white matter blueprints of the whole cortex based on a set of white matter tracts that can be anatomically matched across species. The blueprints provide a common reference space that allows us to navigate between brains of different species, identify homologous cortical areas, or to transform whole cortical maps from one species to the other. Specializations are cast within this framework as deviations between the species’ blueprints. We illustrate how this approach can be used to compare human and macaque brains.
very day, chacma baboons, an old world primate, navigate to and from the safety of their sleeping post and distant foraging or watering sites 1. The decision to move to alternative locations is not simply guided by accumulation of sensory evidence for that choice but by internal representation or memory of the alternative choice's value. The same is true when they move back toward the sleeping post in the evening. While sensory and associative decision-making have been well-studied 2 , less is known about how representations of counterfactual choices-choices not currently taken but which may be taken in the
The great promise of comparative neuroscience is to understand why brains differ by investigating the relations between variations in the organization of different brains, their evolutionary history, and their current ecological niche. For this approach to be successful, the organization of different brains needs to be quantifiable. Here, we present an approach to formally comparing the connectivity of different cortical areas across different brains. We exploit the fact that cortical regions can be characterized by the unique pattern of connectivity, the so-called connectivity fingerprint. By comparing connectivity fingerprints between cortical areas in the human and non-human primate brain we can identify between-species homologs, but also illustrate that is driving differences between species. We illustrate the approach by comparing the organization of the frontal cortex between humans and macaques, showing general similarities combined with some differences in the lateral frontal pole.
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