bioRxiv Science⌕ Search

Biology subjects

van den Brink, R. L.

Publications and source records attributed to van den Brink, R. L..

8 recordsLinked to original sources

Cortex-wide Dynamics of Internal Decisions About Behavioral Context

Many human decisions manifest in the outside world as motor actions. Correspondingly, neural signals reflecting decision formation are expressed in neural populations encoding the final action. Some decisions, however, are internal, shaping overt behavior indirectly through the selection of policies or rules that guide elementary sensory-motor decisions. We studied the human brain dynamics underlying internal decisions about the stimulus-response mapping rule for reporting visual orientation judgments. The rule changed unpredictably in a hidden fashion, and participants tracked it by accumulating ambiguous sensory cues. Computational model-based decoding of source-level magnetoencephalography data uncovered representations of the internal belief about the active rule in many areas, including occipital cortex. These representations exhibited profiles as predicted by normative models and as observed in action-related frontal areas during overt decisions. We conclude that a widely distributed network of cortical areas implements evidence accumulation for internal decisions, and that even visual cortex may represent high-level beliefs.

neuroscience↗

Brainstem arousal systems adaptively shape large-scale cortical interactions for flexible decision-making

Most perceptual decisions entail a flexible mapping from sensory input to motor output. Flexible input-output mapping is reflected in correlated variability within the cortical network involved in perceptual decisions. Here, we tested the idea that brainstem arousal systems are involved in flexible input-output mapping and changes in cortical correlated variability. We combined brainstem fMRI, pupillometry, and time-resolved assessment of the intrinsic correlations between cortical population codes for stimulus and action. Human participants reported the orientation of visual stimuli by button presses, while the required stimulus-response mapping rule could undergo hidden and unpredictable changes. Rule switches evoked brainstem and pupil responses as well as changes in computational model-inferred, latent variables. These variables governed participants rule-switching behavior and pupil responses. Brainstem activity and pupil dilation preceded increases in the strength of correlations between cortical stimulus and action codes. Brainstem arousal systems may promote the reorganization of sensorimotor cortical pathways for flexible decisions.

neuroscience↗

Large-Scale Circuit Configuration for Flexible Sensory-Motor Decisions

Humans and non-human primates can flexibly switch between different arbitrary mappings from sensation to action to solve a cognitive task. It has remained unknown how the brain implements such flexible sensory-motor mapping rules. Here, we uncovered a dynamic reconfiguration of task-specific correlated variability between sensory and motor brain regions. Human participants switched between two rules for reporting visual orientation judgments during fMRI recordings. Rule switches were either signaled explicitly or inferred by the participants from ambiguous cues. We used behavioral modeling to reconstruct the time course of their belief about the active rule. In both contexts, the patterns of correlations between ongoing fluctuations in stimulus- and action-selective activity across visual and action-related brain regions tracked participants belief about the active rule. The rule-specific correlation patterns broke down around the time of behavioral errors. We conclude that internal beliefs about task state are instantiated in brain-wide, selective patterns of correlated variability.

neuroscience↗

Dissociation between catecholamines and acetylcholine in the human cerebral cortex

Influential accounts postulate distinct roles of the catecholamine and acetylcholine neuromodulatory systems in cognition and behavior. But previous work found similar effects of these modulators on the response properties of individual cortical neurons. Here, we report a double dissociation between catecholamine and acetylcholine effects at the level of cortex-wide network interactions in humans. A pharmacological boost of catecholamine levels increased cortex-wide interactions during a visual task, but not rest. Conversely, an acetylcholine-boost decreased correlations during rest, but not task. Cortical circuit modeling explained this dissociation by differential changes in two circuit properties: the local excitation-inhibition balance (more strongly altered by catecholamines) and intracortical transmission (more strongly reduced by acetylcholine). The inferred catecholaminergic mechanism also predicted increased behavioral exploration, which we confirmed in human behavior during both a perceptual and value-based choice task. In sum, we identified specific circuit mechanisms for shaping cortex-wide network interactions and behavior by key neuromodulatory systems.

neuroscience↗

Neuronal timescales are functionally dynamic and shaped by cortical microarchitecture

Complex cognitive functions such as working memory and decision-making require information maintenance over many timescales, from transient sensory stimuli to long-term contextual cues. While theoretical accounts predict the emergence of a corresponding hierarchy of neuronal timescales, direct electrophysiological evidence across the human cortex is lacking. Here, we infer neuronal timescales from invasive intracranial recordings. Timescales increase along the principal sensorimotor-to-association axis across the entire human cortex, and scale with single-unit timescales within macaques. Cortex-wide transcriptomic analysis shows direct alignment between timescales and expression of excitation- and inhibition-related genes, as well as genes specific to voltage-gated transmembrane ion transporters. Finally, neuronal timescales are functionally dynamic: prefrontal cortex timescales expand during working memory maintenance and predict individual performance, while cortex-wide timescales compress with aging. Thus, neuronal timescales follow cytoarchitectonic gradients across the human cortex, and are relevant for cognition in both short- and long-terms, bridging microcircuit physiology with macroscale dynamics and behavior.

neuroscience↗

Temporal expectation hastens sensory encoding but does not affect evidence quality

The ability to predict the timing of forthcoming events, known as temporal expectation, has a strong impact on human information processing. Although there is growing consensus that temporal expectations enhance the speed and accuracy of perceptual decisions, it remains unclear whether they affect the decision process itself, or non-decisional (sensory / motor) processes. Here, healthy human participants (N = 21; 18 female) used predictive auditory cues to anticipate the timing of low-contrast visual stimuli they were required to detect. Modelling of the behavioral data using a prominent sequential sampling model indicated that temporal expectations speeded up non-decisional processes but had no effect on decision formation. Electrophysiological recordings confirmed and extended this result: temporal expectations hastened the onset of a neural signature of decision formation, but had no effect on its build-up rate. Anticipatory alpha-band power was modulated by temporal expectation, and co-varied with intrinsic trial-by-trial variability in behavioral and neural signatures of the onset latency of the decision process. These findings highlight how temporal predictions optimize our interaction with unfolding sensory events. SIGNIFICANCE STATEMENTTemporal expectation enhances performance, but the locus of this effect remains debated. Here, we contrasted the two dominant accounts: enhancement through (1) expedited decision onset, or (2) an increase in the quality of sensory evidence. We manipulated expectations about the onset of a dim visual target using a temporal cueing paradigm, and probed the locus of the expectation effect with two complementary approaches: drift diffusion modeling of behavior, and estimation of the onset and progression of the decision process from a supramodal accumulation-to-bound signal in simultaneously measured EEG signals. Behavioral modeling and neural data provided strong, converging evidence for an account in which temporal expectations enhance perception by speeding up decision onset, without affecting evidence quality.

neuroscience↗

Sustaining attention for a prolonged period of time increases temporal variability in cortical responses

Our ability to stay focused is limited: prolonged performance of a task typically results in mental fatigue and decrements in performance over time. This so-called vigilance decrement has been attributed to depletion of attentional resources, though other factors such as reductions in motivation likely also play a role. In this study, we examined three EEG markers of attentional control, to elucidate which stage of attentional processing is most affected by time-on-task and motivation. To elicit the vigilance decrement, participants performed a sustained attention task for 80 minutes without breaks. After 60 minutes, participants were motivated by an unexpected monetary incentive to increase performance in the final 20 minutes. We found that task performance and self-reported motivation declined rapidly, reaching a stable levels well before the motivation manipulation was introduced. Thereafter, motivation increased back up to the initial level, and remained there for the final 20 minutes. While task performance also increased, it did not return to the initial level, and fell to the lowest level overall during the final 10 minutes. This pattern of performance changes was mirrored by the trial-to-trial consistency of the phase of theta (3-7 Hz) oscillations, an index of the variability in timing of the neural response to the stimulus. As task performance decreased, temporal variability increased, suggesting that attentional stability is crucial for sustained attention performance. The effects of attention on our two other EEG measures--early P1/N1 event-related potentials and pre-stimulus alpha (9-14 Hz) power--did not change with time-on-task or motivation. In sum, these findings show that the vigilance decrement is accompanied by a decline in only some facets of attentional control, which cannot be fully brought back online by increases in motivation. The vigilance decrement might thus not occur due to a single cause, but is likely multifactorial in origin.

neuroscience↗

Amplification and Suppression of Distinct Brain-wide Activity Patterns by Catecholamines

The widely projecting catecholaminergic (norepinephrine and dopamine) neurotransmitter systems profoundly shape the state of neuronal networks in the forebrain. Current models posit that the effects of catecholaminergic modulation on network dynamics are homogenous across the brain. However, the brain is equipped with a variety of catecholamine receptors with distinct functional effects and heterogeneous density across brain regions. Consequently, catecholaminergic effects on brain-wide network dynamics might be more spatially specific than assumed. We tested this idea through the analysis of functional magnetic resonance imaging (fMRI) measurements performed in humans (19 females, 5 males) at rest under pharmacological (atomoxetine-induced) elevation of catecholamine levels. We used a linear decomposition technique to identify spatial patterns of correlated fMRI signal fluctuations that were either increased or decreased by atomoxetine. This yielded two distinct spatial patterns, each expressing reliable and specific drug effects. The spatial structure of both fluctuation patterns resembled the spatial distribution of the expression of catecholamine receptor genes: 1 norepinephrine receptors (for the fluctuation pattern: placebo > atomoxetine), D2-like dopamine receptors (pattern: atomoxetine > placebo), and {beta} norepinephrine receptors (for both patterns, with correlations of opposite sign). We conclude that catecholaminergic effects on the forebrain are spatially more structured than traditionally assumed and at least in part explained by the heterogeneous distribution of various catecholamine receptors. Our findings link catecholaminergic effects on large-scale brain networks to low-level characteristics of the underlying neurotransmitter systems. They also provide key constraints for the development of realistic models of neuromodulatory effects on large-scale brain network dynamics.\n\nSIGNIFICANCE STATEMENTThe catecholamines norepinephrine and dopamine are an important class of modulatory neurotransmitters. Because of the widespread and diffuse release of these neuromodulators, it has commonly been assumed that their effects on neural interactions are homogenous across the brain. Here, we present results from the human brain that challenge this view. We pharmacologically increased catecholamine levels and imaged the effects on the spontaneous covariations between brain-wide fMRI signals at rest. We identified two distinct spatial patterns of covariations: one that was amplified and another that was suppressed by catecholamines. Each pattern was associated with the heterogeneous spatial distribution of the expression of distinct catecholamine receptor genes. Our results provide novel insights into the catecholaminergic modulation of large-scale human brain dynamics.

neuroscience↗