Niels A. Kloosterman

How embodied is perceptual decision making? Evidence for separate processing of perceptual and motor decisions

The extent to which different cognitive processes are “embodied” is widely debated. Previous studies have implicated sensorimotor regions such as lateral intraparietal (LIP) area in perceptual decision making. This has led to the view that perceptual decisions are embodied in the same sensorimotor networks that guide body movements. We use event-related fMRI and effective connectivity analysis to investigate whether the human sensorimotor system implements perceptual decisions. We show that when eye and hand motor preparation is disentangled from perceptual decisions, sensorimotor areas are not involved in accumulating sensory evidence toward a perceptual decision. Instead, inferior frontal cortex increases its effective connectivity with sensory regions representing the evidence, is modulated by the amount of evidence, and shows greater task-positive BOLD responses during the perceptual decision stage. Once eye movement planning can begin, however, an intraparietal sulcus (IPS) area, putative LIP, participates in motor decisions. Moreover, sensory evidence levels modulate decision and motor preparation stages differently in different IPS regions, suggesting functional heterogeneity of the IPS. This suggests that different systems implement perceptual versus motor decisions, using different neural signatures.

Dynamic modulation of decision biases by Brainstem Arousal Systems

Decision-makers often arrive at different choices when faced with repeated presentations of the same evidence. Variability of behavior is commonly attributed to noise in the brain’s decision-making machinery. We hypothesized that phasic responses of brainstem arousal systems are a significant source of this variability. We tracked pupil responses (a proxy of phasic arousal) during sensory-motor decisions in humans, across different sensory modalities and task protocols. Large pupil responses generally predicted a reduction in decision bias. Using fMRI, we showed that the pupil-linked bias reduction was (i) accompanied by a modulation of choice-encoding pattern signals in parietal and prefrontal cortex and (ii) predicted by phasic, pupil-linked responses of a number of neuromodulatory brainstem centers involved in the control of cortical arousal state, including the noradrenergic locus coeruleus. We conclude that phasic arousal suppresses decision bias on a trial-by-trial basis, thus accounting for a significant component of the variability of choice behavior. DOI: http://dx.doi.org/10.7554/eLife.23232.001

The Time Course of Perceptual Grouping in Natural Scenes

Visual perception starts with localized filters that subdivide the image into fragments that undergo separate analyses. The visual system has to reconstruct objects by grouping image fragments that belong to the same object. A widely held view is that perceptual grouping occurs in parallel across the visual scene and without attention. To test this idea, we measured the speed of grouping in pictures of animals and vehicles. In a classification task, these pictures were categorized efficiently. In an image-parsing task, participants reported whether two cues fell on the same or different objects, and we measured reaction times. Despite the participants’ fast object classification, perceptual grouping required more time if the distance between cues was larger, and we observed an additional delay when the cues fell on different parts of a single object. Parsing was also slower for inverted than for upright objects. These results imply that perception starts with rapid object classification and that rapid classification is followed by a serial perceptual grouping phase, which is more efficient for objects in a familiar orientation than for objects in an unfamiliar orientation.

Multiple transient signals in human visual cortex associated with an elementary decision

The cerebral cortex continuously undergoes changes in its state, which are manifested in transient modulations of the cortical power spectrum. Cortical state changes also occur at full wakefulness and during rapid cognitive acts, such as perceptual decisions. Previous studies found a global modulation of beta-band (12–30 Hz) activity in human and monkey visual cortex during an elementary visual decision: reporting the appearance or disappearance of salient visual targets surrounded by a distractor. The previous studies disentangled neither the motor action associated with behavioral report nor other secondary processes, such as arousal, from perceptual decision processing per se. Here, we used magnetoencephalography in humans to pinpoint the factors underlying the beta-band modulation. We found that disappearances of a salient target were associated with beta-band suppression, and target reappearances with beta-band enhancement. This was true for both overt behavioral reports (immediate button presses) and silent counting of the perceptual events. This finding indicates that the beta-band modulation was unrelated to the execution of the motor act associated with a behavioral report of the perceptual decision. Further, changes in pupil-linked arousal, fixational eye movements, or gamma-band responses were not necessary for the beta-band modulation. Together, our results suggest that the beta-band modulation was a top-down signal associated with the process of converting graded perceptual signals into a categorical format underlying flexible behavior. This signal may have been fed back from brain regions involved in decision processing to visual cortex, thus enforcing a “decision-consistent” cortical state. SIGNIFICANCE STATEMENT Elementary visual decisions are associated with a rapid state change in visual cortex, indexed by a modulation of neural activity in the beta-frequency range. Such decisions are also followed by other events that might affect the state of visual cortex, including the motor command associated with the report of the decision, an increase in pupil-linked arousal, fixational eye movements, and fluctuations in bottom-up sensory processing. Here, we ruled out the necessity of these events for the beta-band modulation of visual cortex. We propose that the modulation reflects a decision-related state change, which is induced by the conversion of graded perceptual signals into a categorical format underlying behavior. The resulting decision signal may be fed back to visual cortex.

Humans strategically shift decision bias by flexibly adjusting sensory evidence accumulation in visual cortex

Choice bias, a hallmark of decision-making, is typically conceptualized as an internal reference, or criterion, against which accumulated evidence is compared. Flexible criterion adjustment allows organisms to adapt to the reward structure associated with the choice alternatives, and is assumed to arise from shifts in this reference. Here, in contrast, we show that criterion setting is implemented by modulating evidence accumulation rather than shifting an internal reference. Compared to a conservative criterion, experimentally inducing a liberal criterion during a visual detection task suppressed prestimulus oscillatory 8-12 Hz (alpha) activity in visual cortex, suggesting increased neural excitability. Increased excitability, in turn, boosted stimulus-related 59-100 Hz (gamma) activity by enhancing cortical response gain. Drift diffusion modeling of choice behaviour confirmed that a liberal criterion specifically biases the process of sensory evidence accumulation. Together, these findings provide a unique insight into the neural determinants of decision bias and its flexible adjustment.Biases, systematic tendencies toward one choice option, are hallmarks of decision-making under uncertainty. In perceptual decision-making, bias can be conceptualized as an internal reference to which incoming sensory evidence is compared. This reference, often called criterion, can be flexibly adjusted to match external asymmetries in the payoffs for certain outcomes. Yet, very little is known about how the human brain implements such strategic criterion shifts. Recent studies suggest that spontaneous fluctuations in neural excitability (indexed by suppression of prestimulus alpha-band (8-12 Hz) power in posterior cortex) may impact the criterion. Crucially however, it is currently unknown whether neural excitability and criterion can flexibly and intentionally be adjusted to meet external demands. Here, we experimentally induced criterion shifts in humans through through verbal instruction and asymmetric reward contingencies and show for the first time that neural excitability is enhanced when humans adopt a liberal criterion compared to a more conservative criterion. Moreover, we show how increased excitability boosts subsequent stimulus-related visual cortical EEG activity in the gamma (59-100 Hz) range by enhancing sensory response gain. Drift diffusion modeling of choice behaviour further confirms that a liberal criterion is achieved by biasing the sensory evidence accumulation process towards yes choices. Together, these findings show that humans are able to intentionally and flexibly adapt neural excitability to current task demands, and that such changes in excitability implement criterion shifts by biasing sensory evidence accumulation.

Surprise about sensory event timing drives cortical transients in the beta frequency band

Learning the statistical structure of the environment is crucial for adaptive behavior. Humans and non-human decision-makers seem to track such structure through a process of probabilistic inference, which enables predictions about behaviorally relevant events. Deviations from such predictions cause surprise, which in turn helps improve inference. Surprise about the timing of behaviorally relevant sensory events drives phasic responses of neuromodulatory brainstem systems, which project to the cerebral cortex. Here, we developed a computational model-based magnetoencephalography (MEG) approach for mapping the resulting cortical transients across space, time, and frequency, in the human brain (N=28, 17 female). We used a Bayesian ideal observer model to learn the statistics of the timing of changes in a simple visual detection task. This model yielded quantitative trial-by-trial estimates of temporal surprise. The model-based surprise variable predicted trial-by trial variations in reaction time more strongly than the externally observable interval timings alone. Trial-by-trial variations in surprise were negatively correlated with the power of cortical population activity measured with MEG. This surprise-related power suppression occurred transiently around the behavioral response, specifically in the beta frequency band. It peaked in parietal and prefrontal cortices, remote from the motor cortical suppression of beta power related to overt report (button press) of change detection. Our results indicate that surprise about sensory event timing transiently suppresses ongoing beta-band oscillations in association cortex. This transient suppression of frontal beta-band oscillations might reflect an active reset triggered by surprise, and is in line with the idea that beta-oscillations help maintain cognitive sets. Significance statement The brain continuously tracks the statistical structure of the environment to anticipate behaviorally relevant events. Deviations from such predictions cause surprise, which in turn drives neural activity in subcortical brain regions that project to the cerebral cortex. We used magnetoencephalography in humans to map out surprise-related modulations of cortical population activity across space, time, and frequency. Surprise was elicited by variable timing of visual stimulus changes requiring a behavioral response. Surprise was quantified by means of an ideal observer model. Surprise predicted behavior as well as a transient suppression of beta frequency band oscillations in frontal cortical regions. Our results are in line with conceptual accounts that have linked neural oscillations in the beta-band to the maintenance of cognitive sets.

Humans strategically shift decision bias by flexibly adjusting sensory evidence accumulation in visual cortex (Version posted online April 4, 2018)

Choice bias, a hallmark of decision-making, is typically conceptualized as an internal reference, or criterion, against which accumulated evidence is compared. Flexible criterion adjustment allows organisms to adapt to the reward structure associated with the choice alternatives, and is assumed to arise from shifts in this reference. Here, in contrast, we show that criterion setting is implemented by modulating evidence accumulation rather than shifting an internal reference. Compared to a conservative criterion, experimentally inducing a liberal criterion during a visual detection task suppressed prestimulus oscillatory 8-12 Hz (alpha) activity in visual cortex, suggesting increased neural excitability. Increased excitability, in turn, boosted stimulus-related 59-100 Hz (gamma) activity by enhancing cortical response gain. Drift diffusion modeling of choice behaviour confirmed that a liberal criterion specifically biases the process of sensory evidence accumulation. Together, these findings provide a unique insight into the neural determinants of decision bias and its flexible adjustment.Biases, systematic tendencies toward one choice option, are hallmarks of decision-making under uncertainty. In perceptual decision-making, bias can be conceptualized as an internal reference to which incoming sensory evidence is compared. This reference, often called criterion, can be flexibly adjusted to match external asymmetries in the payoffs for certain outcomes. Yet, very little is known about how the human brain implements such strategic criterion shifts. Recent studies suggest that spontaneous fluctuations in neural excitability (indexed by suppression of prestimulus alpha-band (8-12 Hz) power in posterior cortex) may impact the criterion. Crucially however, it is currently unknown whether neural excitability and criterion can flexibly and intentionally be adjusted to meet external demands. Here, we experimentally induced criterion shifts in humans through through verbal instruction and asymmetric reward contingencies and show for the first time that neural excitability is enhanced when humans adopt a liberal criterion compared to a more conservative criterion. Moreover, we show how increased excitability boosts subsequent stimulus-related visual cortical EEG activity in the gamma (59-100 Hz) range by enhancing sensory response gain. Drift diffusion modeling of choice behaviour further confirms that a liberal criterion is achieved by biasing the sensory evidence accumulation process towards yes choices. Together, these findings show that humans are able to intentionally and flexibly adapt neural excitability to current task demands, and that such changes in excitability implement criterion shifts by biasing sensory evidence accumulation.

Criterion Setting is Implemented through Flexible Adjustment of Neural Excitability in Human Visual Cortex

Choice bias, a hallmark of decision-making, is typically conceptualized as an internal reference, or criterion, against which accumulated evidence is compared. Flexible criterion adjustment allows organisms to adapt to the reward structure associated with the choice alternatives, and is assumed to arise from shifts in this reference. Here, in contrast, we show that criterion setting is implemented by modulating evidence accumulation rather than shifting an internal reference. Compared to a conservative criterion, experimentally inducing a liberal criterion during a visual detection task suppressed prestimulus oscillatory 8-12 Hz (alpha) activity in visual cortex, suggesting increased neural excitability. Increased excitability, in turn, boosted stimulus-related 59-100 Hz (gamma) activity by enhancing cortical response gain. Drift diffusion modeling of choice behaviour confirmed that a liberal criterion specifically biases the process of sensory evidence accumulation. Together, these findings provide a unique insight into the neural determinants of decision bias and its flexible adjustment.Biases, systematic tendencies toward one choice option, are hallmarks of decision-making under uncertainty. In perceptual decision-making, bias can be conceptualized as an internal reference to which incoming sensory evidence is compared. This reference, often called criterion, can be flexibly adjusted to match external asymmetries in the payoffs for certain outcomes. Yet, very little is known about how the human brain implements such strategic criterion shifts. Recent studies suggest that spontaneous fluctuations in neural excitability (indexed by suppression of prestimulus alpha-band (8-12 Hz) power in posterior cortex) may impact the criterion. Crucially however, it is currently unknown whether neural excitability and criterion can flexibly and intentionally be adjusted to meet external demands. Here, we experimentally induced criterion shifts in humans through through verbal instruction and asymmetric reward contingencies and show for the first time that neural excitability is enhanced when humans adopt a liberal criterion compared to a more conservative criterion. Moreover, we show how increased excitability boosts subsequent stimulus-related visual cortical EEG activity in the gamma (59-100 Hz) range by enhancing sensory response gain. Drift diffusion modeling of choice behaviour further confirms that a liberal criterion is achieved by biasing the sensory evidence accumulation process towards yes choices. Together, these findings show that humans are able to intentionally and flexibly adapt neural excitability to current task demands, and that such changes in excitability implement criterion shifts by biasing sensory evidence accumulation.

Criterion Setting Modulates Neural Excitability of Human Visual Cortex

Choice bias, a hallmark of decision-making, is typically conceptualized as an internal reference, or criterion, against which accumulated evidence is compared. Flexible criterion adjustment allows organisms to adapt to the reward structure associated with the choice alternatives, and is assumed to arise from shifts in this reference. Here, in contrast, we show that criterion setting is implemented by modulating evidence accumulation rather than shifting an internal reference. Compared to a conservative criterion, experimentally inducing a liberal criterion during a visual detection task suppressed prestimulus oscillatory 8-12 Hz (alpha) activity in visual cortex, suggesting increased neural excitability. Increased excitability, in turn, boosted stimulus-related 59-100 Hz (gamma) activity by enhancing cortical response gain. Drift diffusion modeling of choice behaviour confirmed that a liberal criterion specifically biases the process of sensory evidence accumulation. Together, these findings provide a unique insight into the neural determinants of decision bias and its flexible adjustment.Biases, systematic tendencies toward one choice option, are hallmarks of decision-making under uncertainty. In perceptual decision-making, bias can be conceptualized as an internal reference to which incoming sensory evidence is compared. This reference, often called criterion, can be flexibly adjusted to match external asymmetries in the payoffs for certain outcomes. Yet, very little is known about how the human brain implements such strategic criterion shifts. Recent studies suggest that spontaneous fluctuations in neural excitability (indexed by suppression of prestimulus alpha-band (8-12 Hz) power in posterior cortex) may impact the criterion. Crucially however, it is currently unknown whether neural excitability and criterion can flexibly and intentionally be adjusted to meet external demands. Here, we experimentally induced criterion shifts in humans through through verbal instruction and asymmetric reward contingencies and show for the first time that neural excitability is enhanced when humans adopt a liberal criterion compared to a more conservative criterion. Moreover, we show how increased excitability boosts subsequent stimulus-related visual cortical EEG activity in the gamma (59-100 Hz) range by enhancing sensory response gain. Drift diffusion modeling of choice behaviour further confirms that a liberal criterion is achieved by biasing the sensory evidence accumulation process towards yes choices. Together, these findings show that humans are able to intentionally and flexibly adapt neural excitability to current task demands, and that such changes in excitability implement criterion shifts by biasing sensory evidence accumulation.