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On the coupling and decoupling of mind wandering and perception: a shared metabolism account

Abstract Introduction Mind wandering (MW) has been associated with reduced responsiveness to external stimuli (“perceptual decoupling”). Conversely, increased perceptual demands of a task result in reduced MW. Here we propose a neurobiological account attributing the mutually-limiting relationship of MW and perception to brain-wide limits on cerebral metabolism. Since overall cerebral metabolism is known to remain constant, despite increased mental task demands, we tested whether increased perceptual processing load in a visual task will result in reduced oxygen metabolism in MW-related medial prefrontal cortex (mPFC) regions. Methods We used broadband near-infrared spectroscopy to measure oxidation states of the cytochrome-c-oxidase enzyme (oxCCO), an intracellular marker of metabolism, in mPFC while sampling participants’ MW experiences during their performance of a visual task of either low (feature search) or high(conjunction search) perceptual load. Results Increased perceptual load in the task resulted in reduced oxCCO signal in mPFC regions related to MW reports. High perceptual load was also found to specifically suppress detailed (and hence more metabolism-demanding) rather than vague MW. Discussion Overall, the results support a shared metabolism account of the relationship between MW and perception and demonstrate that attentional-regulation of metabolism only supports ongoing detailed MW when perceptual processing demands are low.

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Frontal mechanisms underlying primate calls recognition by humans.

The ability to process verbal language seems unique to humans and relies not only on semantics but on other forms of communication such as affective vocalizations, that we share with other primate species-particularly great apes (Hominidae). To better understand these processes at the behavioral and brain level, we asked human participants to categorize vocalizations of four primate species including human, great apes (chimpanzee and bonobo), and monkey (rhesus macaque) during MRI acquisition. Classification was above chance level for all species but bonobo vocalizations. Imaging analyses were computed using a participant-specific, trial-by-trial fitted probability categorization value in a model-based style of data analysis. Model-based analyses revealed the implication of the bilateral orbitofrontal cortex and inferior frontal gyrus pars triangularis (IFGtri) respectively correlating and anti-correlating with the fitted probability of accurate species classification. Further conjunction analyses revealed enhanced activity in a sub-area of the left IFGtri specifically for the accurate classification of chimpanzee calls compared to human voices. Our data-that are controlled for acoustic variability between species-therefore reveal distinct frontal mechanisms that shed light on how the human brain evolved to process vocal signals.

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Detection and characterization of resting state functional networks in squirrel monkey brain.

Resting-state fMRI based on analyzing BOLD signals is widely used to derive functional networks in the brain and how they alter during disease or injury conditions. Resting-state networks can also be used to study brain functional connectomes across species, which provides insights into brain evolution. The squirrel monkey (SM) is a non-human primate (NHP) that is widely used as a preclinical model for experimental manipulations to understand the organization and functioning of the brain. We derived resting-state networks from the whole brain of anesthetized SMs using Independent Component Analysis of BOLD acquisitions. We detected 15 anatomically constrained resting-state networks localized in the cortical and subcortical regions as well as in the white-matter. Networks encompassing visual, somatosensory, executive control, sensorimotor, salience and default mode regions, and subcortical networks including the Hippocampus-Amygdala, thalamus, basal-ganglia and brainstem region correspond well with previously detected networks in humans and NHPs. The connectivity pattern between the networks also agrees well with previously reported seed-based resting-state connectivity of SM brain. This study demonstrates that SMs share remarkable homologous network organization with humans and other NHPs, thereby providing strong support for their suitability as a translational animal model for research and additional insight into brain evolution across species.

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Different patterns of intrinsic functional connectivity at the default mode and attentional networks predict crystalized and fluid abilities in childhood.

Crystallized abilities are skills used to solve problems based on experience, while fluid abilities are linked to reasoning without evoke prior knowledge. To what extent crystallized and fluid abilities involve dissociated or overlapping neural systems is debatable. Due to often deployed small sample sizes or different study settings in prior work, the neural basis of crystallized and fluid abilities in childhood remains largely unknown. Here we analyzed within and between network connectivity patterns from resting-state functional MRI of 2707 children between 9 and 10years from the ABCD study. We hypothesized that differences in functional connectivity at the default mode network (DMN), ventral, and dorsal attentional networks (VAN, DAN) explain differences in fluid and crystallized abilities. We found that stronger between-network connectivity of the DMN and VAN, DMN and DAN, and VAN and DAN predicted crystallized abilities. Within-network connectivity of the DAN predicted both crystallized and fluid abilities. Our findings reveal that crystallized abilities rely on the functional coupling between attentional networks and the DMN, whereas fluid abilities are associated with a focal connectivity configuration at the DAN. Our study provides new evidence into the neural basis of child intelligence and calls for future comparative research in adulthood during neuropsychiatric diseases.

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Methamphetamine enhances neural activation during anticipation of loss in the monetary incentive delay task.

Stimulants like methamphetamine (MA) affect motivated behaviors via actions on circuits mediating mood, attention, and reward. Few studies examined the effects of single doses of stimulants on reward circuits during anticipation and receipt of rewards and losses. Here, we examined the effects of MA (20mg) or placebo in a within-subject, double-blind study with healthy adults (n = 43). During 2 fMRI sessions, participants completed the monetary incentive delay task. Primary outcome measures were BOLD activation in selected regions of interest during anticipation and receipt of monetary rewards and losses. Secondary analyses included behavioral measures, whole brain analysis, and arterial spin labeling. MA produced its expected behavioral effects and increased neural activation in the ventral striatum and anterior insula during anticipation of monetary loss versus non-loss. MA did not affect activation during anticipation of gains, or during receipt of wins or losses. MA significantly reduced cerebral blood flow in the striatum and insula. The present finding that a stimulant enhances the responses of striatal and insular regions to upcoming loss suggests that this system may be sensitive to the salience of upcoming events. The finding adds to a complex body of evidence regarding the effects of stimulant drugs on neural processes during motivated behaviors.

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Structural-and-dynamical similarity predicts compensatory brain areas driving the post-lesion functional recovery mechanism.

The focal lesion alters the excitation-inhibition (E-I) balance and healthy functional connectivity patterns, which may recover over time. One possible mechanism for the brain to counter the insult is global reshaping functional connectivity alterations. However, the operational principles by which this can be achieved remain unknown. We propose a novel equivalence principle based on structural and dynamic similarity analysis to predict whether specific compensatory areas initiate lost E-I regulation after lesion. We hypothesize that similar structural areas (SSAs) and dynamically similar areas (DSAs) corresponding to a lesioned site are the crucial dynamical units to restore lost homeostatic balance within the surviving cortical brain regions. SSAs and DSAs are independent measures, one based on structural similarity properties measured by Jaccard Index and the other based on post-lesion recovery time. We unravel the relationship between SSA and DSA by simulating a whole brain mean field model deployed on top of a virtually lesioned structural connectome from human neuroimaging data to characterize global brain dynamics and functional connectivity at the level of individual subjects. Our results suggest that wiring proximity and similarity are the 2 major guiding principles of compensation-related utilization of hemisphere in the post-lesion functional connectivity re-organization process.

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Increased hippocampal efficiency is associated with greater headache frequency in adolescents with chronic headache.

Adults with chronic headache have altered brain hippocampal efficiency networks. Less is known about the mechanisms underlying chronic headache in youth. In total, 29 youth with chronic headache (10-18years), and 29 healthy, age- and sex-matched controls tracked their headache attacks daily for 1-month period. Following this, they underwent a resting state functional magnetic resonance imaging scan and self-reported on their pubertal status, post-traumatic stress, anxiety, and depression symptoms. Graph-based topological analyses of brain networks, rendering hippocampal efficiency values were performed. T-tests were used to compare hippocampal efficiency metrics between patients and controls. Linear regression was used to examine significant hippocampal efficiency metrics in relation to headache frequency in patients, controlling for age, sex, pubertal status, post-traumatic stress, anxiety, and depression symptoms. Patients had higher right hippocampal global efficiency, shorter right hippocampal path length, and higher right hippocampal clustering coefficient compared to controls (P < 0.05). Higher right hippocampal global efficiency, shorter right hippocampal path length, and higher right hippocampal clustering coefficients were positively associated with greater headache frequency (P < 0.05). The hippocampus is largely involved in memory formation and retrieval, and this data provides additional support for previous findings demonstrating the importance of the hippocampus and pain memories for the chronification of pain.

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