ABSTRACT
Previous research has highlighted the role of glutamate and gamma-aminobutyric acid (GABA) in perceptual, cognitive, and motor tasks. However, the exact involvement of these neurochemical mechanisms in the chain of information processing, and across human development, is unclear. In a cross-sectional longitudinal design, we used a computational approach to dissociate cognitive, decision, and visuomotor processing in 293 individuals spanning early childhood to adulthood. We found that glutamate and GABA within the intraparietal sulcus (IPS) explained unique variance in visuomotor processing, with higher glutamate predicting poorer visuomotor processing in younger participants but better visuomotor processing in mature participants, while GABA showed the opposite pattern. These findings, which were neurochemically, neuroanatomically and functionally specific, were replicated ~21 mo later and were generalized in two further different behavioral tasks. Using resting functional MRI, we revealed that the relationship between IPS neurochemicals and visuomotor processing is mediated by functional connectivity in the visuomotor network. We then extended our findings to high-level cognitive behavior by predicting fluid intelligence performance. We present evidence that fluid intelligence performance is explained by IPS GABA and glutamate and is mediated by visuomotor processing. However, this evidence was obtained using an uncorrected alpha and needs to be replicated in future studies. These results provide an integrative biological and psychological mechanistic explanation that links cognitive processes and neurotransmitters across human development and establishes their potential involvement in intelligent behavior.
Subject(s)
Cognition , Magnetic Resonance Imaging , Child, Preschool , Humans , Child , Adolescent , Young Adult , Cross-Sectional Studies , Magnetic Resonance Imaging/methods , Glutamates , Intelligence , gamma-Aminobutyric AcidABSTRACT
The distance effect states that the closer two compared magnitudes (e.g., two numbers, physical attractiveness in two faces), the more difficult the comparison, and the greater the activity of the frontoparietal control network. However, it is unclear whether this network is also recruited to the same extent when we perform ingroup and outgroup beauty comparisons and whether the activation of these networks is tracked by interindividual variation in the perceptions we hold about an outgroup. We recorded brain activity with fMRI, where participants compared the beauty of two women ostensibly either from their ingroup or from an outgroup. Low-distance conditions produced longer response times than the high-distance conditions, and this was found in both the ingroup and outgroup conditions. However, our neuroimaging analyses revealed that the left IFG/anterior insula showed the classic distance effect only during ingroup processing but not during outgroup processing. Notably, interaction-specific activity within the left IFG/anterior insula was related to perceptions of outgroup homogeneity assessed via a questionnaire. This set of findings reveals the dynamic role of the prefrontal cortex and its interplay with perceptions of outgroup homogeneity in shaping ingroup and outgroup decision-making.
Subject(s)
Prefrontal Cortex , Humans , Female , Reaction Time , Prefrontal Cortex/diagnostic imagingABSTRACT
The survival and well-being of humans require solving the patch-switching problem: we must decide when to stop collecting rewards in a current patch and travel somewhere else where gains may be higher. Previous studies suggested that frontal regions are underpinned by several processes in the context of foraging decisions such as tracking task difficulty, and/or the value of exploring the environment. To dissociate between these processes, participants completed an fMRI patch-switching learning task inspired by behavioral ecology. By analyzing >11,000 trials collected across 21 participants, we found that the activation in the cingulate cortex was closely related to several patch-switching-related variables including the decision to leave the current patch, the encounter of a new patch, the harvest value, and the relative forage value. Learning-induced changes in the patch-switching threshold were tracked by activity within frontoparietal regions including the superior frontal gyrus and angular gyrus. Our findings suggest that frontoparietal regions shape patch-switching learning apart from encoding classical non-learning foraging processes. These findings provide a novel neurobiological understanding of how learning emerges neurocomputationally shaping patch-switching behavior with implications in real-life choices such as job selection and pave the way for future studies to probe the causal role of these neurobiological mechanisms.
Subject(s)
Frontal Lobe , Gyrus Cinguli , Humans , Frontal Lobe/physiology , Gyrus Cinguli/diagnostic imaging , Gyrus Cinguli/physiology , Prefrontal Cortex , Learning , Magnetic Resonance ImagingABSTRACT
Receiving feedback from our environment that informs us about the outcomes of our actions helps us assess our abilities (e.g., metacognition) and to flexibly adapt our behavior, consequently increasing our chances of success. However, a detailed examination of the effect of feedback on the brain activation during perceptual and confidence judgments as well as the interrelations between perceptual accuracy, prospective and retrospective confidence remains unclear. Here we used functional magnetic resonance imaging (fMRI) to examine the neural response to feedback valence and source in visual contrast discrimination together with prospective confidence judgments at the beginning of each block and retrospective confidence judgments after every decision. Positive feedback was associated with higher activation (or lower deactivation depending on the area) in areas previously involved in attention, performance monitoring and visual regions during the perceptual judgment than during the confidence judgment. Changes in prospective confidence were positively related to changes in perceptual accuracy as well as to the corresponding retrospective confidence. Thus, feedback information impacted multiple, qualitatively different brain processing states, and we also revealed the dynamic interplay between prospective, perceptual accuracy and retrospective self-assessment.
Subject(s)
Metacognition , Decision Making/physiology , Feedback , Humans , Judgment , Magnetic Resonance Imaging/methods , Metacognition/physiology , Prospective Studies , Retrospective Studies , Visual PerceptionABSTRACT
The increased prevalence of test anxiety in our competitive society makes it a health issue of public concern. However, its neurobiological basis, especially during the years of formal education, is currently scant. Previous research has highlighted the association between neural excitation/inhibition balance and psychopathology and disease. We examined whether the glutamate/GABA profile tracks test anxiety levels in development, using a cross-sectional and longitudinal design in a cohort spanning from early childhood to early adulthood (N = 289), reassessed approximately 21 months later (N = 194). We used magnetic resonance spectroscopy to noninvasively quantify glutamate and gamma-Aminobutyric acid (GABA) levels in the intraparietal sulcus (IPS) and the middle frontal gyrus. We show that the glutamate/GABA balance within the IPS relates to current individual variation in test anxiety levels and predict future test anxiety approximately 21 months later. Critically, this relationship was observed during early childhood but not during the later developmental stages. Our results extend the use of the excitation/inhibition balance framework to characterize the psychopathology mechanisms of test anxiety, an underexplored yet widespread and debilitating condition that can impact early child development. Our findings provide a better understanding of the neurotransmitter basis underlying the emergence of anxiety disorders during development.
Subject(s)
Glutamic Acid , Test Anxiety , Adult , Child , Child, Preschool , Cross-Sectional Studies , Humans , Longitudinal Studies , gamma-Aminobutyric AcidABSTRACT
Several scientific, engineering, and medical advancements are based on breakthroughs made by people who excel in mathematics. Our current understanding of the underlying brain networks stems primarily from anatomical and functional investigations, but our knowledge of how neurotransmitters subserve numerical skills, the building block of mathematics, is scarce. Using 1H magnetic resonance spectroscopy (N = 54, 3T, semi-LASER sequence, TE = 32 ms, TR = 3.5 s), the study examined the relation between numerical skills and the brain's major inhibitory (GABA) and excitatory (glutamate) neurotransmitters. A negative association was found between the performance in a number sequences task and the resting concentration of GABA within the left intraparietal sulcus (IPS), a key region supporting numeracy. The relation between GABA in the IPS and number sequences was specific to (1) parietal but not frontal regions and to (2) GABA but not glutamate. It was additionally found that the resting functional connectivity of the left IPS and the left superior frontal gyrus was positively associated with number sequences performance. However, resting GABA concentration within the IPS explained number sequences performance above and beyond the resting frontoparietal connectivity measure. Our findings further motivate the study of inhibition mechanisms in the human brain and significantly contribute to our current understanding of numerical cognition's biological bases.
Subject(s)
Mathematics , Parietal Lobe/metabolism , Problem Solving/physiology , gamma-Aminobutyric Acid/metabolism , Adolescent , Female , Humans , Magnetic Resonance Imaging , Magnetic Resonance Spectroscopy , Male , Neural Pathways/diagnostic imaging , Neural Pathways/metabolism , Parietal Lobe/diagnostic imaging , Young AdultABSTRACT
Previous research has highlighted the role of glutamate and gamma-aminobutyric acid (GABA) in learning and plasticity. What is currently unknown is how this knowledge translates to real-life complex cognitive abilities that emerge slowly and how the link between these neurotransmitters and human learning and plasticity is shaped by development. While some have suggested a generic role of glutamate and GABA in learning and plasticity, others have hypothesized that their involvement shapes sensitive periods during development. Here we used a cross-sectional longitudinal design with 255 individuals (spanning primary school to university) to show that glutamate and GABA in the intraparietal sulcus explain unique variance both in current and future mathematical achievement (approximately 1.5 years). Furthermore, our findings reveal a dynamic and dissociable role of GABA and glutamate in predicting learning, which is reversed during development, and therefore provide novel implications for models of learning and plasticity during childhood and adulthood.
Subject(s)
Glutamic Acid/metabolism , Learning , Neuronal Plasticity , gamma-Aminobutyric Acid/metabolism , Adolescent , Adult , Child , Cognition , Cross-Sectional Studies , Female , Humans , Magnetic Resonance Imaging , MaleABSTRACT
Formal education has a long-term impact on an individual's life. However, our knowledge of the effect of a specific lack of education, such as in mathematics, is currently poor but is highly relevant given the extant differences between countries in their educational curricula and the differences in opportunities to access education. Here we examined whether neurotransmitter concentrations in the adolescent brain could classify whether a student is lacking mathematical education. Decreased γ-aminobutyric acid (GABA) concentration within the middle frontal gyrus (MFG) successfully classified whether an adolescent studies math and was negatively associated with frontoparietal connectivity. In a second experiment, we uncovered that our findings were not due to preexisting differences before a mathematical education ceased. Furthermore, we showed that MFG GABA not only classifies whether an adolescent is studying math or not, but it also predicts the changes in mathematical reasoning â¼19 mo later. The present results extend previous work in animals that has emphasized the role of GABA neurotransmission in synaptic and network plasticity and highlight the effect of a specific lack of education on MFG GABA concentration and learning-dependent plasticity. Our findings reveal the reciprocal effect between brain development and education and demonstrate the negative consequences of a specific lack of education during adolescence on brain plasticity and cognitive functions.
Subject(s)
Achievement , Brain/growth & development , Mathematics/education , Adolescent , Behavior , Biomarkers/metabolism , Brain/diagnostic imaging , Female , Frontal Lobe/diagnostic imaging , Frontal Lobe/growth & development , Humans , Magnetic Resonance Imaging , Male , Neuronal Plasticity/physiology , gamma-Aminobutyric Acid/metabolismABSTRACT
Neurochemical profile and brain connectivity are both critical aspects of brain function. However, our knowledge of their interplay across development is currently poor. We combined single-voxel magnetic resonance spectroscopy and resting functional magnetic resonance imaging in a cross-sectional sample spanning from childhood to adulthood which was reassessed in ~1.5 years (N = 293). We revealed the developmental trajectories of 20 neurochemicals in two key developmental brain regions (the intraparietal sulcus, IPS, and the middle frontal gyrus, MFG). We found that certain neurochemicals exhibited similar developmental trajectories across the two regions, while other trajectories were region-specific. Crucially, we mapped the connectivity of the brain regions IPS and MFG to the rest of the brain across development as a function of regional glutamate and GABA concentration. We demonstrated that glutamate concentration within the IPS is modulated by age in explaining IPS connectivity with frontal, temporal and parietal regions. In mature participants, higher glutamate within the IPS was related to more negative connectivity while the opposite pattern was found for younger participants. Our findings offer specific developmental insights on the interplay between the brain's resting activity and the glutamatergic system both of which are crucial for regulating normal functioning and are dysregulated in several clinical conditions.
Subject(s)
Cerebral Cortex/physiology , Connectome , Glutamic Acid/metabolism , Human Development/physiology , Magnetic Resonance Imaging , Magnetic Resonance Spectroscopy , Nerve Net/physiology , Adolescent , Adult , Cerebral Cortex/diagnostic imaging , Cerebral Cortex/metabolism , Child , Cross-Sectional Studies , Female , Humans , Male , Nerve Net/diagnostic imaging , Nerve Net/metabolism , Young AdultABSTRACT
Working memory (WM) capacity, the amount of information one can hold online in mind, has a central role in cognition. Previous electrophysiological and imaging studies revealed the pivotal role of persistent activity within parietal and frontal regions as the neural foundations underpinning WM capacity. The best candidate molecules determining persistent activity are the brain's major excitatory and inhibitory neurotransmitters, glutamate and gamma-aminobutyric acid (GABA), respectively. However, our knowledge of these neurophysiological determinants in forming WM capacity is still poor. Using magnetic resonance spectroscopy (MRS), we examined the contribution of glutamate and GABA within the left intraparietal sulcus (IPS) and the left inferior/middle frontal gyrus (FG) in tracking WM capacity. A positive association was found between glutamate within the left IPS and WM capacity. By utilising resting-state functional MRI, we identified a negative association between parieto-cingulate connectivity and WM capacity. Individual variation in parieto-cingulate connectivity was explained by glutamatergic concentration in the IPS. Moreover, we found that parieto-cingulate connectivity mediated the relationship between interparietal sulcus glutamate and WM capacity. This set of findings reveals a novel mechanistic insight by which glutamatergic concentration within the IPS shapes WM capacity via parieto-cingulate connectivity.
Subject(s)
Memory, Short-Term , Parietal Lobe , Brain Mapping , Magnetic Resonance Imaging , Magnetic Resonance Spectroscopy , Parietal Lobe/diagnostic imaging , Prefrontal CortexABSTRACT
Cognitive control is a pivotal aspect of cognition and it is impaired in many clinical populations. To date, several distinct types of cognitive control have been proposed, and prior work demonstrated the instrumental role of basal ganglia, frontal and parietal regions. However, the role of the structural variation of these regions in cognitive control functions is poorly understood. Here, we examined in 39 adults the association between regional brain volume and three major types of cognitive control: (i) stimulus updating, (ii) task-switching, and (iii) distractor filtering. The volume of the globus pallidus was positively correlated with individual variation in task-switching , and was anatomically specific to the left hemisphere. Importantly, this region did not track performance in distractor filtering or stimulus updating. We then aimed to use transcranial direct current stimulation to target the left midline subcortical structures. However, we did not find an effect on task-switching. While the null effect in the brain stimulation prevents us from drawing causal inference from the role of globus pallidus on task-switching, our structural results reveal a novel and highly specific neurostructural mechanism for task-switching and provide a further understanding of the link between cognitive control functions and the human brain.
Subject(s)
Attention/physiology , Executive Function/physiology , Globus Pallidus/anatomy & histology , Memory, Short-Term/physiology , Psychomotor Performance/physiology , Adult , Female , Functional Laterality/physiology , Globus Pallidus/diagnostic imaging , Humans , Magnetic Resonance Imaging , Male , Middle Aged , Placebos , Prefrontal Cortex/physiology , Transcranial Direct Current Stimulation , Young AdultABSTRACT
Working memory, the ability to maintain and manipulate information over seconds, is central to cognition and it is impaired in many clinical populations. However, our knowledge of the structural properties associated with individual variation in visuospatial working memory capacity is currently poor. Across two locations (Stockholm and Oxford), we examined how regional surface area and cortical thickness in frontal and parietal regions were related to visuospatial working memory capacity. We found a negative association between visuospatial working memory capacity and the surface area of the left frontal pole across both locations, and this finding was consistently present in each of the two locations separately. Importantly, this association was specific to (i) the surface area (not cortical thickness), (ii) the left side of the brain, (iii) and the visuospatial rather than the verbal modality. This result reveals a novel and highly specific neurobiological association with visuospatial working memory which could be further explored in studies with a wider range of psychological tests and in clinical populations.
Subject(s)
Frontal Lobe , Memory, Short-Term , Cognition , Frontal Lobe/diagnostic imaging , Humans , Parietal LobeABSTRACT
The continuous balancing of the risks and benefits of exploiting known options or exploring new opportunities is essential to human life. We forage for new opportunities when they are deemed to be more attractive than the available option, but this decision to forage also entails costs. People differ in their propensity to exploit or forage, and both the social circumstances and our individual value orientations are likely influences. Here, participants made foraging decisions for themselves and for a charity of their choice in two paradigms: one that features two distinct modes of decision-making (foraging vs classical economic decision-making) and one which is more directly related to the classical animal foraging and ethology literature. Across both paradigms, individuals who possessed a stronger self-focused value orientation obtained more rewards when they were allowed to forage for themselves rather than the charity. Neuroimaging during the tasks revealed that this effect was associated with activity in the dorsal anterior cingulate cortex (dACC) in that more self-focused individuals showed lower activity in dACC for the self-condition relative to the other condition. This evidence reveals a dynamic interplay between foraging outcomes and the higher-order value system of individuals.
Subject(s)
Ego , Feeding Behavior/physiology , Social Behavior , Adolescent , Adult , Decision Making , Female , Gyrus Cinguli/diagnostic imaging , Gyrus Cinguli/physiology , Humans , Individuality , Magnetic Resonance Imaging , Male , Neuroimaging , Reward , Social Values , Young AdultABSTRACT
Herein, the authors compare morbidity in men who underwent both transrectal ultrasound-guided (TRUS) prostate biopsy and transperineal mapping biopsy (TPMB) at two institutions with extensive experience in both procedures. We also identified strategies and predictive factors to reduce morbidity for both procedures. In our study, 379 men from two institutions, of which 265 (69.9%) had a prior TRUS-guided biopsy, also had TPMB performed via a template with biopsies taken at 5-mm intervals. Men in the TRUS group had a median of 12 cores sampled whereas the TPMB group had 51.5 (range, 16-151). The median biopsy density was 1.1 core/cc prostate volume. Median age and prostate-specific antigen (PSA) level were 65 years (range, 34-86) and 5.5 ng/mL (range, 0.02-118). Of these men, 11 of 265 (4.2%) who had TRUS biopsy developed urinary tract infection compared with 3 of 379 (0.79%) of those with mapping biopsy. Infection was 14.8% in TRUS biopsy group with 13 or more cores versus 2.9% in those with 12 or less (OR, 5.8; 95% CI, 1.6-21.2; P = 0.003). No men developed retention after TRUS biopsy whereas 30 of 379 (7.9%) did following TPMB. Older age, larger prostate volume (PV), and higher core number were associated with retention. On linear regression only age (P = 0.010) and PV (P = 0.016) remained as significant associations. Men older than 65 years had 12.8% versus 3.9% (OR, 3.7; 95% CI, 1.6-8.4, P = 0.001) and PV greater than 42 cc had 13.4% versus 2.7% (OR, 5.7; 95% CI, 2.1-15.1) retention incidence. In the present study TPMB is rarely associated with infection (0.78%) but more commonly with urinary retention (7.9%). Men older than 65 years and with PV greater than 42 cc were at four to five times greater retention risk. Consideration should be given to discharging these men with a urinary catheter following TPMB.
ABSTRACT
Human values guide behavior and the smooth functioning of societies. Schwartz's circumplex model of values predicts a sinusoidal waveform in relations between ratings of the importance of diverse human value types (e.g., achievement, benevolence) and any variables psychologically relevant to them. In this neuroimaging study, we examined these nonlinear associations between values types and brain structure. In 85 participants, we found the predicted sinusoidal relationship between ratings of values types and two measures of white matter (WM), volume and myelin volume fraction, as well as for grey matter (GM) parameters in several frontal regions. These effects reveal new functional associations for structural brain parameters and provide a novel cross-validation of Schwartz's model. Moreover, the sinusoidal waveform test can be applied to other circumplex models in social, affective and cognitive neuroscience.
Subject(s)
Brain/diagnostic imaging , Social Values , Adult , Female , Gray Matter/diagnostic imaging , Humans , Magnetic Resonance Imaging , Male , Models, Psychological , White Matter/diagnostic imaging , Young AdultABSTRACT
Human values and personality have been shown to share genetic variance in twin studies. However, there is a lack of evidence about the genetic components of this association. This study examined the interplay between genes, values and personality in the case of neuroticism, because polygenic scores were available for this personality trait. First, we replicated prior evidence of a positive association between the polygenic neuroticism score (PNS) and neuroticism. Second, we found that the PNS was significantly associated with the whole human value space in a sinusoidal waveform that was consistent with Schwartz's circular model of human values. These results suggest that it is useful to consider human values in the analyses of genetic contributions to personality traits. They also pave the way for an investigation of the biological mechanisms contributing to human value orientations.
Subject(s)
Anxiety Disorders/genetics , Social Values , Adult , Female , Genetic Variation , Humans , Male , Neuroticism , Personality/geneticsABSTRACT
Can subjective belief about one's own perceptual competence change one's perception? To address this question, we investigated the influence of self-efficacy on sensory discrimination in two low-level visual tasks: contrast and orientation discrimination. We utilised a pre-post manipulation approach whereby two experimental groups (high and low self-efficacy) and a control group made objective perceptual judgments on the contrast or the orientation of the visual stimuli. High and low self-efficacy were induced by the provision of fake social-comparative performance feedback and fictional research findings. Subsequently, the post-manipulation phase was performed to assess changes in visual discrimination thresholds as a function of the self-efficacy manipulations. The results showed that the high self-efficacy group demonstrated greater improvement in visual discrimination sensitivity compared to both the low self-efficacy and control groups. These findings suggest that subjective beliefs about one's own perceptual competence can affect low-level visual processing.