Separate Neural Mechanisms Research Articles

Action expectancy modulates activity in the mirror neuron system and mentalizing system

Action understanding involves two distinct processing levels that engage separate neural mechanisms: perception of concrete kinematic information and recognition of abstract action intentions. The mirror neuron system and the mentalizing system have both been linked to concrete action and abstract information processing, but their specific roles remain debatable. Here, we conducted a functional magnetic resonance imaging study with 26 participants who passively observed expected and unexpected actions. We performed whole-brain activation, region of interest, and effective connectivity analyses to investigate the neural correlates of these actions. Whole-brain activation analyses revealed that expected actions were associated with increased activation in the left medial superior frontal gyrus, while unexpected actions were linked to heightened activity in the left supramarginal gyrus, left superior parietal lobule, right inferior temporal gyrus, and left middle frontal gyrus. Region of interest analyses demonstrated that the left ventral premotor cortex exhibited greater activation during the observation of expected actions compared to unexpected actions, while the left inferior frontal gyrus, left superior parietal lobule, and left precuneus showed stronger activation during the observation of unexpected actions. Effective connectivity was observed between the left ventral premotor cortex and the left angular gyrus, left intraparietal sulcus, left dorsal premotor cortex, and left ventromedial prefrontal cortex with the middle frontal gyrus when observing unexpected, but not expected, actions. These findings suggest that expected actions are primarily processed by the mirror neuron system, whereas unexpected actions engage both the mirror neuron system and the mentalizing system, with these systems playing complementary roles in the understanding of unexpected actions.

Semantic cognition versus numerical cognition: a topographical perspective.

Semantic cognition and numerical cognition are dissociable faculties with separable neural mechanisms. However, recent advances in the cortical topography of the temporal and parietal lobes have revealed a common organisational principle for the neural representations of semantics and numbers. We discuss their convergence and divergence through the prism of topography.

Distinct neuronal representation of small and large numbers in the human medial temporal lobe.

Whether small numerical quantities are represented by a special subitizing system that is distinct from a large-number estimation system has been debated for over a century. Here we show that two separate neural mechanisms underlie the representation of small and large numbers. We performed single neuron recordings in the medial temporal lobe of neurosurgical patients judging numbers. We found a boundary in neuronal coding around number 4 that correlates with the behavioural transition from subitizing to estimation. In the subitizing range, neurons showed superior tuning selectivity accompanied by suppression effects suggestive of surround inhibition as a selectivity-increasing mechanism. In contrast, tuning selectivity decreased with increasing numbers beyond 4, characterizing a ratio-dependent number estimation system. The two systems with the coding boundary separating them were also indicated using decoding and clustering analyses. The identified small-number subitizing system could be linked to attention and working memory that show comparable capacity limitations.

Split-Belt Treadmill Adaptation Improves Spatial and Temporal Gait Symmetry in People with Multiple Sclerosis

Multiple sclerosis (MS) is a neurodegenerative disease characterized by degradation of the myelin sheath resulting in impaired neural communication throughout the body. As a result, most people with MS (PwMS) experience gait asymmetries between their legs leading to an increased risk of falls. Recent work indicates that split-belt treadmill adaptation, where the speed of each leg is controlled independently, can decrease gait asymmetries for other neurodegenerative impairments. The purpose of this study was to test the efficacy of split-belt treadmill training to improve gait symmetry in PwMS. In this study, 35 PwMS underwent a 10 min split-belt treadmill adaptation paradigm, with the faster paced belt moving under the more affected limb. Step length asymmetry (SLA) and phase coordination index (PCI) were the primary outcome measures used to assess spatial and temporal gait symmetries, respectively. It was predicted that participants with a worse baseline symmetry would have a greater response to split-belt treadmill adaptation. Following this adaptation paradigm, PwMS experienced aftereffects that improved gait symmetry, with a significant difference between predicted responders and nonresponders in both SLA and PCI change (p < 0.001). Additionally, there was no correlation between SLA and PCI change. These findings suggest that PwMS retain the ability for gait adaptation, with those most asymmetrical at baseline demonstrating the greatest improvement, and that there may be separate neural mechanisms for spatial and temporal locomotor adjustments.

Uncovering neural distinctions and commodities between two creativity subsets: A meta-analysis of fMRI studies in divergent thinking and insight using activation likelihood estimation.

The dual‐process theory that two different systems of thought coexist in creative thinking has attracted considerable attention. In the field of creative thinking, divergent thinking (DT) is the ability to produce multiple solutions to open‐ended problems in a short time. It is mainly considered an associative and fast process. Meanwhile, insight, the new and unexpected comprehension of close‐ended problems, is frequently marked as a deliberate and time‐consuming thinking process requiring concentrated effort. Previous research has been dedicated to revealing their separate neural mechanisms, while few studies have compared their differences and similarities at the brain level. Therefore, the current study applied Activation Likelihood Estimation to decipher common and distinctive neural pathways that potentially underlie DT and insight. We selected 27 DT studies and 30 insight studies for retrospective meta‐analyses. Initially, two single analyses with follow‐up contrast and conjunction analyses were performed. The single analyses showed that DT mainly involved the inferior parietal lobe (IPL), cuneus, and middle frontal gyrus (MFG), while the precentral gyrus, inferior frontal gyrus (IFG), parahippocampal gyrus (PG), amygdala (AMG), and superior parietal lobe were engaged in insight. Compared to insight, DT mainly led to greater activation in the IPL, the crucial part of the default mode network. However, insight caused more significant activation in regions related to executive control functions and emotional responses, such as the IFG, MFG, PG, and AMG. Notably, the conjunction analysis detected no overlapped areas between DT and insight. These neural findings implicate that various neurocognitive circuits may support DT and insight.

Temporal dynamics of the neural representation of hue and luminance polarity

Hue and luminance contrast are basic visual features. Here we use multivariate analyses of magnetoencephalography data to investigate the timing of the neural computations that extract them, and whether they depend on common neural circuits. We show that hue and luminance-contrast polarity can be decoded from MEG data and, with lower accuracy, both features can be decoded across changes in the other feature. These results are consistent with the existence of both common and separable neural mechanisms. The decoding time course is earlier and more temporally precise for luminance polarity than hue, a result that does not depend on task, suggesting that luminance contrast is an updating signal that separates visual events. Meanwhile, cross-temporal generalization is slightly greater for representations of hue compared to luminance polarity, providing a neural correlate of the preeminence of hue in perceptual grouping and memory. Finally, decoding of luminance polarity varies depending on the hues used to obtain training and testing data. The pattern of results is consistent with observations that luminance contrast is mediated by both L-M and S cone sub-cortical mechanisms.

Deep networks trained to recognize facial expressions predict ventral face-selective ECoG responses as well as networks trained to recognize identity

Faces are a rich source of information about people’s identity and their facial expressions. Recognition of identity and expression have been traditionally thought to be performed by separate neural mechanisms. However, recent neuroimaging studies suggest that recognition of identity and expressions may not be as disjointed as originally thought: valence can be decoded from patterns of response in the FFA (Skerry & Saxe 2014), a brain region previously implicated in identity recognition. If ventral temporal face-selective regions are specialized for the recognition of identity, we would expect deep networks trained to recognize identity to provide a better model of neural responses in these regions as compared to networks trained to recognize facial expressions. In this study, we used electrocorticography (ECoG) to test this prediction, comparing the similarity between neural representations and representations from deep networks trained to recognize either identity or expressions. Patients were shown face images from the Karolinska Directed Emotional Faces database (Lundqvist et al., 1998) while intracranial recordings from ventral temporal brain regions were collected. Using temporal representational similarity analysis for each electrode over sliding temporal windows, we compared representational dissimilarity matrices (RDMs) obtained from the ECoG data to RDMs obtained from one model trained on expression recognition and one model trained on identity recognition. Similarity between RDMs from different layers of the DNNs and the RDMs obtained from ECoG data at different time windows was also evaluated. RDMs from networks trained to recognize expression and those trained to recognize identity were equally able to explain ventral temporal regions when presented with face stimuli. These results provide further support for the presence of both identity and expression information within common brain regions and suggest that ventral temporal regions may not be exclusively optimized for identity recognition.

Separable neural mechanisms support intentional forgetting and thought substitution

Psychological and neuroscientific experiments have established that people can intentionally forget information via different strategies: direct suppression and thought substitution. However, few studies have directly compared the effectiveness of these strategies in forgetting specific items, and it remains an open question if the neural mechanisms supporting these strategies differ. Here, we developed a novel item-method directed forgetting paradigm with Remember, Forget, and Imagine cues, and recorded EEG to directly compare these strategies. Behaviorally, Forget and Imagine cues produced similar forgetting compared to Remember cues, but through separable neural processes; Forget cues elicited frontal oscillatory power changes that were predictive of future forgetting, whereas item-cue representational similarity was predictive of later accuracy for Imagine cues. These results suggest that both strategies can lead to intentional forgetting, but directed forgetting may rely on frontally-mediated suppression, while thought substitution may lead to contextual shifting, impairing successful retrieval.

Growing evidence for separate neural mechanisms for attention and consciousness.

Our conscious experience of the world seems to go in lockstep with our attentional focus: We tend to see, hear, taste, and feel what we attend to, and vice versa. This tight coupling between attention and consciousness has given rise to the idea that these two phenomena are indivisible. In the late 1950s, the honoree of this special issue, Charles Eriksen, was among a small group of early pioneers that sought to investigate whether a transient increase in overall level of attention (alertness) in response to a noxious stimulus can be decoupled from conscious perception using experimental techniques. Recent years saw a similar debate regarding whether attention and consciousness are two dissociable processes. Initial evidence that attention and consciousness are two separate processes primarily rested on behavioral data. However, the past couple of years witnessed an explosion of studies aimed at testing this conjecture using neuroscientific techniques. Here we provide an overview of these and related empirical studies on the distinction between the neuronal correlates of attention and consciousness, and detail how advancements in theory and technology can bring about a more detailed understanding of the two. We argue that the most promising approach will combine ever-evolving neurophysiological and interventionist tools with quantitative, empirically testable theories of consciousness that are grounded in a mathematically formalized understanding of phenomenology.

Action-induced changes in the perceived temporal features of visual events

Perceived duration can be subject to deviations around the time of a voluntary action. Whether the mechanisms underlying action-induced visual duration effects are effector-specific or require a more generalized action-linked multimodal calibration with the transient visual system, however, is a question yet to be answered. Here, we investigate this using dynamic visual stimuli presented as contingent upon the execution of an arbitrarily associated voluntary manual response. Our results demonstrate that the duration of intervals with arbitrarily associated keypress–visual event pair is perceived as shorter than the duration in a pure visual condition, where the same stimuli are rather passively observed without the execution of a concurrent action. Whereas the control experiments show that motor memory and attention cannot explain the action-induced changes in perceived temporal features, action-induced changes in perceived speed are dissociated from those in perceived duration, and that the duration compression disappears using isoluminant or static stimuli, which together provide evidence that these two effects can be modulated in the motion-processing units, although via separate neural mechanisms.

Comparison of Food Cue-Evoked and Resting-State Functional Connectivity in Obesity.

Obesity is associated with differences in task-evoked and resting-state functional brain connectivity (FC). However, no studies have compared obesity-related differences in FC evoked by high-calorie food cues from that observed at rest. Such a comparison could improve our understanding of the neural mechanisms of reward valuation and decision making in the context of obesity. The sample included 122 adults (78% female; mean age = 44.43 [8.67] years) with body mass index (BMI) in the overweight or obese range (mean = 31.28 [3.92] kg/m). Participants completed a functional magnetic resonance imaging scan that included a resting period followed by a visual food cue task. Whole-brain FC analyses examined seed-to-voxel signal covariation during the presentation of high-calorie food and at rest using seeds located in the left and right orbitofrontal cortex, left hippocampus, and left dorsomedial prefrontal cortex. For all seeds examined, BMI was associated with stronger FC during the presentation of high-calorie food, but weaker FC at rest. Regions exhibiting BMI-related modulation of signal coherence in the presence of palatable food cues were largely located within the default mode network (z range = 2.34-4.91), whereas regions exhibiting BMI-related modulation of signal coherence at rest were located within the frontostriatal and default mode networks (z range = 3.05-4.11). All FC results exceeded a voxelwise threshold of p < .01 and cluster-defining familywise error threshold of p < .05. These dissociable patterns of FC may suggest separate neural mechanisms contributing to variation in distinct cognitive, psychological, or behavioral domains that may be related to individual differences in risk for obesity.

Effect of cone spectral topography on chromatic detection sensitivity.

The spatial and spectral topography of the cone mosaic set the limits for detection and discrimination of chromatic sinewave gratings. Here, we sought to compare the spatial characteristics of mechanisms mediating hue perception against those mediating chromatic detection in individuals with known spectral topography and with optical aberrations removed with adaptive optics. Chromatic detection sensitivity in general exceeded previous measurements and decreased monotonically for increasingly skewed cone spectral compositions. The spatial grain of hue perception was significantly coarser than chromatic detection, consistent with separate neural mechanisms for color vision operating at different spatial scales.

Separable neural mechanisms for the pleiotropic association of copy number variants with neuropsychiatric traits

22q11.2, 15q13.3, and 1q21.1 microdeletions attract considerable interest by conferring high risk for a range of neuropsychiatric disorders, including schizophrenia and autism. A fundamental open question is whether divergent or convergent neural mechanisms mediate this genetic pleiotropic association with the same behavioral phenotypes. We use a combination of rodent microdeletion models with high-field neuroimaging to perform a comparative whole-brain characterization of functional and structural mechanisms linked to high-risk states. Resting-state functional and structural magnetic resonance imaging data were acquired on mice carrying heterozygous microdeletions in 22q11.2 (N = 12), 15q13.3 (N = 11), and 1q21.1 (N = 11) loci. We performed network-based statistic, graph, and morphometric analyses. The three microdeletions did not share significant systems-level features. Instead, morphometric analyses revealed microcephaly in 1q21.1 and macrocephaly in 15q13.3 deletions, whereas cerebellar volume was specifically reduced in 22q11.2 deletion. In function, 22q11.2 deletion mice showed widespread cortical hypoconnectivity, accompanied by opposing hyperconnectivity in dopaminergic pathways, which was confirmed by graph analysis. 1q21.1 exhibited distinct changes in posterior midbrain morphology and function, especially in periaqueductal gray, whereas 15q13.3 demonstrated alterations in auditory/striatal system. The combination of cortical hypoconnectivity and dopaminergic hyperconnectivity and reduced cerebellum in 22q11.2 deletion mirrors key neurodevelopmental features of schizophrenia, whereas changes in midbrain and auditory/striatal morphology and topology in 1q21.1 and 15q13.3 rather indicate focal processes possibly linked to the emergence of abnormal salience perception and hallucinations. In addition to insights into pathophysiological processes in these microdeletions, our results establish the general point that microdeletions might increase risk for overlapping neuropsychiatric phenotypes through separable neural mechanisms.

Walking and finger tapping can be done with independent rhythms

Rhythmic movements occur in many aspects of daily life. Examples include clapping the hands and walking. The production of two independent rhythms with multiple limbs is considered to be extremely difficult. In the present study we evaluated whether two different, independent rhythms that involved finger tapping and walking could be produced. In Experiment I, twenty subjects that had no experience of musical instrument training performed rhythmic finger tapping with the right index finger and one of four different lower limb movements; (1) self-paced walking, (2) given-paced walking, (3) alternative bilateral heel tapping from a sitting position, and (4) unilateral heel tapping with the leg ipsilateral to the tapping finger from a sitting position. The target intervals of finger tapping and heel strikes for walking step/heel tapping were set at 375 ms and 600 ms, respectively. The even distribution of relative phases between instantaneous finger tapping and heel strike was taken as the criteria of independency for the two rhythms. In the self-paced walking and given-paced walking tasks, 16 out of 20 subjects successfully performed finger tapping and walking with independent rhythms without any special practice. On the other hand, in the bipedal heels striking and unipedal heel striking tasks 19 subjects failed to perform the two movements independently, falling into interrelated rhythms with the ratio mostly being 2:1. In Experiment II, a similar independency of finger tapping and walking at a given pace was observed for heel strike intervals of 400, 600, and 800 ms, as well as at the constant 375 ms for finger tapping. These results suggest that finger tapping and walking are controlled by separate neural control mechanisms, presumably with a supra-spinal locus for finger tapping, and a spinal location for walking.

Salience-Driven Value Construction for Adaptive Choice under Risk.

Decisions we face in real life are inherently risky and can result in one of many possible outcomes. However, most of what we know about choice under risk is based on studies that use options with only two possible outcomes (simple gambles), so it remains unclear how the brain constructs reward values for more complex risky options faced in real life. To address this question, we combined experimental and modeling approaches to examine choice between pairs of simple gambles and pairs of three-outcome gambles in male and female human subjects. We found that subjects evaluated individual outcomes of three-outcome gambles by multiplying functions of reward magnitude and probability. To construct the overall value of each gamble, however, most subjects differentially weighted possible outcomes based on either reward magnitude or probability. These results reveal a novel dissociation between how reward information is processed when evaluating complex gambles: valuation of each outcome is based on a combination of reward information whereas weighting of possible outcomes mainly relies on a single piece of reward information. We show that differential weighting of possible outcomes could enable subjects to make decisions more easily and quickly. Together, our findings reveal a plausible mechanism for how salience, in terms of possible reward magnitude or probability, can influence the construction of subjective values for complex gambles. They also point to separable neural mechanisms for how reward value controls choice and attention to allow for more adaptive decision making under risk.SIGNIFICANCE STATEMENT Real-life decisions are inherently risky and can result in one of many possible outcomes, but how does the brain integrate information from all these outcomes to make decisions? To address this question, we examined choice between pairs of gambles with multiple outcomes using various computational models. We found that subjects evaluated individual outcomes by multiplying functions of reward magnitude and probability. To construct the overall value of each gamble, however, they differentially weighted possible outcomes based on either reward magnitude or probability. By doing so, they were able to make decisions more easily and quickly. Our findings illustrate how salience, in terms of possible reward magnitude or probability, can influence the construction of subjective values for more adaptive choice.

The time course of different surround suppression mechanisms.

What we see depends on the spatial context in which it appears. Previous work has linked the suppression of perceived contrast by surrounding stimuli to reduced neural responses in early visual cortex. This surround suppression depends on at least two separable neural mechanisms, “low-level” and “higher level,” which can be differentiated by their response characteristics. We used electroencephalography to demonstrate for the first time that human occipital neural responses show evidence of these two suppression mechanisms. Eighteen adults (10 women, 8 men) each participated in three experimental sessions, in which they viewed visual stimuli through a mirror stereoscope. The first session was used to identify the C1 component, while the second and third comprised the main experiment. Event-related potentials were measured in response to center gratings either with no surround or with surrounding gratings oriented parallel or orthogonal, and presented in either the same eye (monoptic) or the opposite eye (dichoptic). We found that the earliest component of an event-related potential (C1; ∼60 ms) was suppressed by surrounding stimuli, but that suppression did not depend on surround configuration. This suggests a suppression mechanism that is not tuned for relative orientation acting on the earliest cortical response to the target. A later response component (N1; ∼160 ms) showed stronger suppression for parallel and monoptic surrounds, consistent with our earlier psychophysical results and a second form of suppression that is binocular and orientation tuned. We conclude that these two forms of surround suppression have distinct response time courses in the human visual system, which can be differentiated using electrophysiology.

Neural Correlates of Consumers Perceiving the Stereotypes of Brand Personality: An Event-Related Potentials Study

Behavioral studies show that the personalities of Chinese traditional and fashionable brands are obviously different, namely a stereotype of personality. It is unclear how the personality evaluations of those brands are processed. This paper aims to explore the neural activities associated with words describing the brand names and its personality evaluations using event-related potentials (ERPs). A word-pair paradigm is used, the first word is a brand name from one of two categories (traditional and fashionable category), and the second word is a personality evaluation either in clemency or trend dimension (the special personality of Chinese brands). Recipients are asked to judge whether the personality evaluations are consistent with the brand names, while ERPs are recorded synchronously. Through the behavior data of reaction times and ERPs components, we conclude that the N400 serves as an index of a mismatch between the stereotypes of the brand and its personality evaluations, while the LPP reflects the consumers’ emotional attitudes in the process of the recalling of brand personality. It seems that the N400 and LPP are driven by separate neural mechanisms. The results verify the stereotypes of brand personality from the perspective of neural activities, and shed new light on the cultivation, monitoring and evaluation of brand personality.

Neural correlates of effort-based valuation with prospective choices

How is effort integrated in value-based decision-making? Animal models and human neuroimaging studies primarily linked the anterior cingulate cortex (ACC) and ventral striatum (VS) to the integration of effort in valuation. Other studies demonstrated the role of these regions in invigoration to effort demands, thus it is hard to separate the neural activity linked to anticipation and subjective valuation from actual performance. Here, we studied the neural basis of effort valuation separated from performance. We scanned forty participants with fMRI, while they were asked to accept or reject monetary gambles that could be resolved with future performance of a familiar grip force effort challenge or a fixed risk prospect. Participants' willingness to accept prospective gambles reflected discounting of values by physical effort and risk. Choice-locked neural activation in contralateral primary sensory cortex and ventromedial prefrontal cortex (vmPFC) tracked the magnitude of prospective effort the participants faced, independent of choice time and monetary stakes. Estimates of subjective value discounted by effort were found to be tracked by the activation of a network of regions common to valuation under risk and delay, including vmPFC, VS and sensorimotor cortex. Together, our findings show separate neural mechanisms underlying prospective effort and actual effort performance.

Maturation trajectories of cortical resting-state networks depend on the mediating frequency band

The functional significance of resting state networks and their abnormal manifestations in psychiatric disorders are firmly established, as is the importance of the cortical rhythms in mediating these networks. Resting state networks are known to undergo substantial reorganization from childhood to adulthood, but whether distinct cortical rhythms, which are generated by separable neural mechanisms and are often manifested abnormally in psychiatric conditions, mediate maturation differentially, remains unknown. Using magnetoencephalography (MEG) to map frequency band specific maturation of resting state networks from age 7 to 29 in 162 participants (31 independent), we found significant changes with age in networks mediated by the beta (13–30 Hz) and gamma (31–80 Hz) bands. More specifically, gamma band mediated networks followed an expected asymptotic trajectory, but beta band mediated networks followed a linear trajectory. Network integration increased with age in gamma band mediated networks, while local segregation increased with age in beta band mediated networks. Spatially, the hubs that changed in importance with age in the beta band mediated networks had relatively little overlap with those that showed the greatest changes in the gamma band mediated networks. These findings are relevant for our understanding of the neural mechanisms of cortical maturation, in both typical and atypical development.

Suppression and facilitation of human neural responses.

Efficient neural processing depends on regulating responses through suppression and facilitation of neural activity. Utilizing a well-known visual motion paradigm that evokes behavioral suppression and facilitation, and combining five different methodologies (behavioral psychophysics, computational modeling, functional MRI, pharmacology, and magnetic resonance spectroscopy), we provide evidence that challenges commonly held assumptions about the neural processes underlying suppression and facilitation. We show that: (1) both suppression and facilitation can emerge from a single, computational principle - divisive normalization; there is no need to invoke separate neural mechanisms, (2) neural suppression and facilitation in the motion-selective area MT mirror perception, but strong suppression also occurs in earlier visual areas, and (3) suppression is not primarily driven by GABA-mediated inhibition. Thus, while commonly used spatial suppression paradigms may provide insight into neural response magnitudes in visual areas, they should not be used to infer neural inhibition.