RESUMEN
The 40â Hz auditory steady-state response (ASSR), an oscillatory brain response to periodically modulated auditory stimuli, is a promising, noninvasive physiological biomarker for schizophrenia and related neuropsychiatric disorders. The 40â Hz ASSR might be amplified by synaptic interactions in cortical circuits, which are, in turn, disturbed in neuropsychiatric disorders. Here, we tested whether the 40â Hz ASSR in the human auditory cortex depends on two key synaptic components of neuronal interactions within cortical circuits: excitation via N-methyl-aspartate glutamate (NMDA) receptors and inhibition via gamma-amino-butyric acid (GABA) receptors. We combined magnetoencephalography (MEG) recordings with placebo-controlled, low-dose pharmacological interventions in the same healthy human participants (13 males, 7 females). All participants exhibited a robust 40â Hz ASSR in auditory cortices, especially in the right hemisphere, under a placebo. The GABAA receptor-agonist lorazepam increased the amplitude of the 40â Hz ASSR, while no effect was detectable under the NMDA blocker memantine. Our findings indicate that the 40â Hz ASSR in the auditory cortex involves synaptic (and likely intracortical) inhibition via the GABAA receptor, thus highlighting its utility as a mechanistic signature of cortical circuit dysfunctions involving GABAergic inhibition.
Asunto(s)
Corteza Auditiva , Potenciales Evocados Auditivos , Neuronas GABAérgicas , Magnetoencefalografía , Humanos , Corteza Auditiva/efectos de los fármacos , Corteza Auditiva/fisiología , Masculino , Femenino , Adulto , Potenciales Evocados Auditivos/efectos de los fármacos , Potenciales Evocados Auditivos/fisiología , Neuronas GABAérgicas/fisiología , Neuronas GABAérgicas/efectos de los fármacos , Adulto Joven , Inhibición Neural/fisiología , Inhibición Neural/efectos de los fármacos , Estimulación AcústicaRESUMEN
Aging is accompanied by a decline of working memory, an important cognitive capacity that involves stimulus-selective neural activity that persists after stimulus presentation. Here, we unraveled working memory dynamics in older human adults (male and female) including those diagnosed with mild cognitive impairment (MCI) using a combination of behavioral modeling, neuropsychological assessment, and MEG recordings of brain activity. Younger adults (male and female) were studied with behavioral modeling only. Participants performed a visuospatial delayed match-to-sample task under systematic manipulation of the delay and distance between sample and test stimuli. Their behavior (match/nonmatch decisions) was fit with a computational model permitting the dissociation of noise in the internal operations underlying the working memory performance from a strategic decision threshold. Task accuracy decreased with delay duration and sample/test proximity. When sample/test distances were small, older adults committed more false alarms than younger adults. The computational model explained the participants' behavior well. The model parameters reflecting internal noise (not decision threshold) correlated with the precision of stimulus-selective cortical activity measured with MEG during the delay interval. The model uncovered an increase specifically in working memory noise in older compared with younger participants. Furthermore, in the MCI group, but not in the older healthy controls, internal noise correlated with the participants' clinically assessed cognitive integrity. Our results are consistent with the idea that the stability of working memory contents deteriorates in aging, in a manner that is specifically linked to the overall cognitive integrity of individuals diagnosed with MCI.
Asunto(s)
Envejecimiento , Encéfalo , Magnetoencefalografía , Memoria a Corto Plazo , Humanos , Masculino , Femenino , Memoria a Corto Plazo/fisiología , Anciano , Envejecimiento/fisiología , Envejecimiento/psicología , Adulto , Persona de Mediana Edad , Adulto Joven , Encéfalo/fisiología , Disfunción Cognitiva/fisiopatología , Disfunción Cognitiva/psicología , Cognición/fisiología , Pruebas Neuropsicológicas , Anciano de 80 o más Años , Modelos NeurológicosRESUMEN
While functional magnetic resonance imaging (fMRI) at ultra-high field (7 T) promises a general increase in sensitivity compared to lower field strengths, the benefits may be most pronounced for specific applications. The current study aimed to evaluate the relative benefit of 7 over 3 T fMRI for the assessment of responses evoked in different brain regions by a well-controlled cognitive task. At 3 and 7 T, the same participants made challenging perceptual decisions about visual motion combined with monetary rewards for correct choices. Previous work on this task has extensively characterized the underlying cognitive computations and single-cell responses in cortical and subcortical structures. We quantified the evoked fMRI responses in extrastriate visual cortical areas, the striatum, and the brainstem during the decision interval and the post-feedback interval of the task. The dependence of response amplitudes on field strength during the decision interval differed between cortical, striatal, and brainstem regions, with a generally bigger 7 versus 3 T benefit in subcortical structures. We also found stronger responses during relatively easier than harder decisions at 7 T for dopaminergic midbrain nuclei, in line with reward expectation. Our results demonstrate the potential of 7 T fMRI for illuminating the contribution of small brainstem nuclei to the orchestration of cognitive computations in the human brain.
Asunto(s)
Tronco Encefálico , Cuerpo Estriado , Toma de Decisiones/fisiología , Neuroimagen Funcional , Imagen por Resonancia Magnética , Percepción de Movimiento/fisiología , Recompensa , Corteza Visual , Adulto , Tronco Encefálico/diagnóstico por imagen , Tronco Encefálico/fisiología , Cuerpo Estriado/diagnóstico por imagen , Cuerpo Estriado/fisiología , Femenino , Humanos , Masculino , Corteza Visual/diagnóstico por imagen , Corteza Visual/fisiología , Adulto JovenRESUMEN
Central to human and animal cognition is the ability to learn from feedback in order to optimize future rewards. Such a learning signal might be encoded and broadcasted by the brain's arousal systems, including the noradrenergic locus coeruleus. Pupil responses and the positive slow wave component of event-related potentials reflect rapid changes in the arousal level of the brain. Here, we ask whether and how these variables may reflect surprise: the mismatch between one's expectation about being correct and the outcome of a decision, when expectations fluctuate due to internal factors (e.g., engagement). We show that during an elementary decision task in the face of uncertainty both physiological markers of phasic arousal reflect surprise. We further show that pupil responses and slow wave event-related potential are unrelated to each other and that prediction error computations depend on feedback awareness. These results further advance our understanding of the role of central arousal systems in decision-making under uncertainty.
Asunto(s)
Nivel de Alerta/fisiología , Encéfalo/fisiología , Toma de Decisiones/fisiología , Potenciales Evocados/fisiología , Retroalimentación Formativa , Reflejo Pupilar/fisiología , Adolescente , Electroencefalografía , Femenino , Humanos , Aprendizaje , Masculino , Pupila/fisiología , Incertidumbre , Adulto JovenRESUMEN
Many decisions result from the accumulation of decision-relevant information (evidence) over time. Even when maximizing decision accuracy requires weighting all the evidence equally, decision-makers often give stronger weight to evidence occurring early or late in the evidence stream. Here, we show changes in such temporal biases within participants as a function of intermittent judgments about parts of the evidence stream. Human participants performed a decision task that required a continuous estimation of the mean evidence at the end of the stream. The evidence was either perceptual (noisy random dot motion) or symbolic (variable sequences of numbers). Participants also reported a categorical judgment of the preceding evidence half-way through the stream in one condition or executed an evidence-independent motor response in another condition. The relative impact of early versus late evidence on the final estimation flipped between these two conditions. In particular, participants' sensitivity to late evidence after the intermittent judgment, but not the simple motor response, was decreased. Both the intermittent response as well as the final estimation reports were accompanied by nonluminance-mediated increases of pupil diameter. These pupil dilations were bigger during intermittent judgments than simple motor responses and bigger during estimation when the late evidence was consistent than inconsistent with the initial judgment. In sum, decisions activate pupil-linked arousal systems and alter the temporal weighting of decision evidence. Our results are consistent with the idea that categorical choices in the face of uncertainty induce a change in the state of the neural circuits underlying decision-making.NEW & NOTEWORTHY The psychology and neuroscience of decision-making have extensively studied the accumulation of decision-relevant information toward a categorical choice. Much fewer studies have assessed the impact of a choice on the processing of subsequent information. Here, we show that intermittent choices during a protracted stream of input reduce the sensitivity to subsequent decision information and transiently boost arousal. Choices might trigger a state change in the neural machinery for decision-making.
Asunto(s)
Toma de Decisiones/fisiología , Juicio/fisiología , Conceptos Matemáticos , Percepción de Movimiento/fisiología , Desempeño Psicomotor/fisiología , Psicofísica , Percepción Espacial/fisiología , Adulto , Humanos , Pupila/fisiología , Adulto JovenRESUMEN
The ascending modulatory systems of the brain stem are powerful regulators of global brain state. Disturbances of these systems are implicated in several major neuropsychiatric disorders. Yet, how these systems interact with specific neural computations in the cerebral cortex to shape perception, cognition, and behavior remains poorly understood. Here, we probed into the effect of two such systems, the catecholaminergic (dopaminergic and noradrenergic) and cholinergic systems, on an important aspect of cortical computation: its intrinsic variability. To this end, we combined placebo-controlled pharmacological intervention in humans, recordings of cortical population activity using magnetoencephalography (MEG), and psychophysical measurements of the perception of ambiguous visual input. A low-dose catecholaminergic, but not cholinergic, manipulation altered the rate of spontaneous perceptual fluctuations as well as the temporal structure of "scale-free" population activity of large swaths of the visual and parietal cortices. Computational analyses indicate that both effects were consistent with an increase in excitatory relative to inhibitory activity in the cortical areas underlying visual perceptual inference. We propose that catecholamines regulate the variability of perception and cognition through dynamically changing the cortical excitation-inhibition ratio. The combined readout of fluctuations in perception and cortical activity we established here may prove useful as an efficient and easily accessible marker of altered cortical computation in neuropsychiatric disorders.
Asunto(s)
Catecolaminas/fisiología , Corteza Cerebral/fisiología , Percepción Visual/fisiología , Inhibidores de Captación Adrenérgica/farmacología , Clorhidrato de Atomoxetina/farmacología , Mapeo Encefálico , Corteza Cerebral/efectos de los fármacos , Humanos , Magnetoencefalografía/métodos , Modelos Neurológicos , Estimulación Luminosa , Placebos , PsicofísicaRESUMEN
Perceptual decision-making is biased by previous events, including the history of preceding choices: observers tend to repeat (or alternate) their judgments of the sensory environment more often than expected by chance. Computational models postulate that these so-called choice history biases result from the accumulation of internal decision signals across trials. Here, we provide psychophysical evidence for such a mechanism and its adaptive utility. Male and female human observers performed different variants of a challenging visual motion discrimination task near psychophysical threshold. In a first experiment, we decoupled categorical perceptual choices and motor responses on a trial-by-trial basis. Choice history bias was explained by previous perceptual choices, not motor responses, highlighting the importance of internal decision signals in action-independent formats. In a second experiment, observers performed the task in stimulus environments containing different levels of autocorrelation and providing no external feedback about choice correctness. Despite performing under overall high levels of uncertainty, observers adjusted both the strength and the sign of their choice history biases to these environments. When stimulus sequences were dominated by either repetitions or alternations, the individual degree of this adjustment of history bias was about as good a predictor of individual performance as individual perceptual sensitivity. The history bias adjustment scaled with two proxies for observers' confidence about their previous choices (accuracy and reaction time). Together, our results are consistent with the idea that action-independent, confidence-modulated decision variables are accumulated across choices in a flexible manner that depends on decision-makers' model of their environment.SIGNIFICANCE STATEMENT Decisions based on sensory input are often influenced by the history of one's preceding choices, manifesting as a bias to systematically repeat (or alternate) choices. We here provide support for the idea that such choice history biases arise from the context-dependent accumulation of a quantity referred to as the decision variable: the variable's sign dictates the choice and its magnitude the confidence about choice correctness. We show that choices are accumulated in an action-independent format and a context-dependent manner, weighted by the confidence about their correctness. This confidence-weighted accumulation of choices enables decision-makers to flexibly adjust their behavior to different sensory environments. The bias adjustment can be as important for optimizing performance as one's sensitivity to the momentary sensory input.
Asunto(s)
Adaptación Psicológica/fisiología , Conducta de Elección/fisiología , Toma de Decisiones/fisiología , Adulto , Discriminación en Psicología/fisiología , Ambiente , Retroalimentación Psicológica , Femenino , Humanos , Masculino , Percepción de Movimiento/fisiología , Observación , Desempeño Psicomotor/fisiología , Tiempo de Reacción/fisiología , Incertidumbre , Adulto JovenRESUMEN
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 homogeneous 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 brainwide network dynamics might be more spatially specific than assumed. We tested this idea through the analysis of 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: α1 norepinephrine receptors (for the fluctuation pattern: placebo > atomoxetine), D2-like dopamine receptors (pattern: atomoxetine > placebo), and ß 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.SIGNIFICANCE STATEMENT The 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 homogeneous 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 brainwide 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.
Asunto(s)
Encéfalo/fisiología , Catecolaminas/fisiología , Conectoma , Inhibidores de Captación Adrenérgica/farmacología , Clorhidrato de Atomoxetina/farmacología , Química Encefálica , Estudios Cruzados , Conjuntos de Datos como Asunto , Método Doble Ciego , Femenino , Neuroimagen Funcional , Humanos , Imagen por Resonancia Magnética , Masculino , Proteínas del Tejido Nervioso/análisis , Proteínas del Tejido Nervioso/genética , Receptores de Catecolaminas/análisis , Receptores de Catecolaminas/genética , DescansoRESUMEN
Learning the statistical structure of the environment is crucial for adaptive behavior. Humans and nonhuman 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.
Asunto(s)
Anticipación Psicológica/fisiología , Ritmo beta/fisiología , Modelos Neurológicos , Modelos Psicológicos , Percepción del Tiempo/fisiología , Adulto , Teorema de Bayes , Corteza Cerebral/fisiología , Femenino , Humanos , Magnetoencefalografía , Masculino , Persona de Mediana Edad , Percepción Visual/fisiología , Adulto JovenRESUMEN
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.
Asunto(s)
Nivel de Alerta/fisiología , Ritmo beta/fisiología , Toma de Decisiones/fisiología , Red Nerviosa/fisiología , Corteza Visual/fisiología , Percepción Visual/fisiología , Adulto , Movimientos Oculares/fisiología , Femenino , Fijación Ocular/fisiología , Humanos , Masculino , Persona de Mediana EdadRESUMEN
At any time, we are processing thousands of stimuli, but only few of them will be remembered hours or days later. Is there any way to predict which ones? Here, we tested whether the pupil response to ongoing stimuli, an indicator of physiological arousal known to be relevant for memory formation, is a reliable predictor of long-term memory for these stimuli, over at least 1 day. Pupil dilation was tracked while participants performed visual and auditory encoding tasks. Memory was tested immediately after encoding and 24 hr later. Irrespective of the encoding modality, trial-by-trial variations in pupil dilation predicted reliably which stimuli were recalled in the immediate and 24 hr-delayed tests, in particular for emotionally arousing stimuli. These results show that our eyes may provide a window into the formation of long-term memories. Furthermore, our findings underline the important role of central arousal systems in the rapid formation of memories in the brain, possibly by gating synaptic plasticity mechanisms in the neocortex.
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Nivel de Alerta/fisiología , Emociones/fisiología , Memoria a Largo Plazo/fisiología , Memoria a Corto Plazo/fisiología , Recuerdo Mental/fisiología , Reconocimiento Visual de Modelos/fisiología , Pupila/fisiología , Percepción del Habla/fisiología , Adolescente , Adulto , Femenino , Humanos , Masculino , Adulto JovenRESUMEN
UNLABELLED: The brain commonly exhibits spontaneous (i.e., in the absence of a task) fluctuations in neural activity that are correlated across brain regions. It has been established that the spatial structure, or topography, of these intrinsic correlations is in part determined by the fixed anatomical connectivity between regions. However, it remains unclear which factors dynamically sculpt this topography as a function of brain state. Potential candidate factors are subcortical catecholaminergic neuromodulatory systems, such as the locus ceruleus-norepinephrine system, which send diffuse projections to most parts of the forebrain. Here, we systematically characterized the effects of endogenous central neuromodulation on correlated fluctuations during rest in the human brain. Using a double-blind placebo-controlled crossover design, we pharmacologically increased synaptic catecholamine levels by administering atomoxetine, an NE transporter blocker, and examined the effects on the strength and spatial structure of resting-state MRI functional connectivity. First, atomoxetine reduced the strength of inter-regional correlations across three levels of spatial organization, indicating that catecholamines reduce the strength of functional interactions during rest. Second, this modulatory effect on intrinsic correlations exhibited a substantial degree of spatial specificity: the decrease in functional connectivity showed an anterior-posterior gradient in the cortex, depended on the strength of baseline functional connectivity, and was strongest for connections between regions belonging to distinct resting-state networks. Thus, catecholamines reduce intrinsic correlations in a spatially heterogeneous fashion. We conclude that neuromodulation is an important factor shaping the topography of intrinsic functional connectivity. SIGNIFICANCE STATEMENT: The human brain shows spontaneous activity that is strongly correlated across brain regions. The factors that dynamically sculpt these inter-regional correlation patterns are poorly understood. Here, we test the hypothesis that they are shaped by the catecholaminergic neuromodulators norepinephrine and dopamine. We pharmacologically increased synaptic catecholamine levels and measured the resulting changes in intrinsic fMRI functional connectivity. At odds with common understanding of catecholamine function, we found (1) overall reduced inter-regional correlations across several levels of spatial organization; and (2) a remarkable spatial specificity of this modulatory effect. Our results identify norepinephrine and dopamine as important factors shaping intrinsic functional connectivity and advance our understanding of catecholamine function in the central nervous system.
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Neuronas Adrenérgicas/fisiología , Catecolaminas/metabolismo , Corteza Cerebral/fisiología , Conectoma/métodos , Neuronas Dopaminérgicas/fisiología , Red Nerviosa/fisiología , Adulto , Método Doble Ciego , Humanos , Imagen por Resonancia Magnética/métodos , Masculino , Vías Nerviosas/fisiología , Efecto Placebo , Descanso/fisiología , Adulto JovenRESUMEN
Cognition results from interactions among functionally specialized but widely distributed brain regions; however, neuroscience has so far largely focused on characterizing the function of individual brain regions and neurons therein. Here we discuss recent studies that have instead investigated the interactions between brain regions during cognitive processes by assessing correlations between neuronal oscillations in different regions of the primate cerebral cortex. These studies have opened a new window onto the large-scale circuit mechanisms underlying sensorimotor decision-making and top-down attention. We propose that frequency-specific neuronal correlations in large-scale cortical networks may be 'fingerprints' of canonical neuronal computations underlying cognitive processes.
Asunto(s)
Mapeo Encefálico , Encéfalo/citología , Red Nerviosa/fisiología , Neuronas/fisiología , Animales , Encéfalo/irrigación sanguínea , Encéfalo/fisiología , Cognición/fisiología , Humanos , Red Nerviosa/citología , Vías Nerviosas/irrigación sanguínea , Vías Nerviosas/fisiología , Neuronas/clasificaciónRESUMEN
Perceptual confidence refers to the degree to which we believe in the accuracy of our percepts. Signal detection theory suggests that perceptual confidence is computed from an internal "decision variable," which reflects the amount of available information in favor of one or another perceptual interpretation of the sensory input. The neural processes underlying these computations have, however, remained elusive. Here, we used fMRI and multivariate decoding techniques to identify regions of the human brain that encode this decision variable and confidence during a visual motion discrimination task. We used observers' binary perceptual choices and confidence ratings to reconstruct the internal decision variable that governed the subjects' behavior. A number of areas in prefrontal and posterior parietal association cortex encoded this decision variable, and activity in the ventral striatum reflected the degree of perceptual confidence. Using a multivariate connectivity analysis, we demonstrate that patterns of brain activity in the right ventrolateral prefrontal cortex reflecting the decision variable were linked to brain signals in the ventral striatum reflecting confidence. Our results suggest that the representation of perceptual confidence in the ventral striatum is derived from a transformation of the continuous decision variable encoded in the cerebral cortex.
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Conducta de Elección/fisiología , Toma de Decisiones/fisiología , Emociones/fisiología , Percepción de Movimiento/fisiología , Percepción/fisiología , Percepción Visual/fisiología , Adolescente , Adulto , Mapeo Encefálico , Corteza Cerebral/fisiología , Femenino , Humanos , Masculino , Corteza Prefrontal/fisiología , Adulto JovenRESUMEN
A number of studies have shown that pupil size increases transiently during effortful decisions. These decision-related changes in pupil size are mediated by central neuromodulatory systems, which also influence the internal state of brain regions engaged in decision making. It has been proposed that pupil-linked neuromodulatory systems are activated by the termination of decision processes, and, consequently, that these systems primarily affect the postdecisional brain state. Here, we present pupil results that run contrary to this proposal, suggesting an important intradecisional role. We measured pupil size while subjects formed protracted decisions about the presence or absence ("yes" vs. "no") of a visual contrast signal embedded in dynamic noise. Linear systems analysis revealed that the pupil was significantly driven by a sustained input throughout the course of the decision formation. This sustained component was larger than the transient component during the final choice (indicated by button press). The overall amplitude of pupil dilation during decision formation was bigger before yes than no choices, irrespective of the physical presence of the target signal. Remarkably, the magnitude of this pupil choice effect (yes > no) reflected the individual criterion: it was strongest in conservative subjects choosing yes against their bias. We conclude that the central neuromodulatory systems controlling pupil size are continuously engaged during decision formation in a way that reveals how the upcoming choice relates to the decision maker's attitude. Changes in brain state seem to interact with biased decision making in the face of uncertainty.
Asunto(s)
Conducta de Elección/fisiología , Toma de Decisiones , Pupila/fisiología , Adolescente , Adulto , Conducta/fisiología , Sesgo , Femenino , Humanos , Masculino , Análisis y Desempeño de Tareas , Factores de Tiempo , Adulto JovenRESUMEN
Conscious perception sometimes fluctuates strongly, even when the sensory input is constant. For example, in motion-induced blindness (MIB), a salient visual target surrounded by a moving pattern suddenly disappears from perception, only to reappear after some variable time. Whereas such changes of perception result from fluctuations of neural activity, mounting evidence suggests that the perceptual changes, in turn, may also cause modulations of activity in several brain areas, including visual cortex. In this study, we asked whether these latter modulations might affect the subsequent dynamics of perception. We used magnetoencephalography (MEG) to measure modulations in cortical population activity during MIB. We observed a transient, retinotopically widespread modulation of beta (12-30 Hz)-frequency power over visual cortex that was closely linked to the time of subjects' behavioral report of the target disappearance. This beta modulation was a top-down signal, decoupled from both the physical stimulus properties and the motor response but contingent on the behavioral relevance of the perceptual change. Critically, the modulation amplitude predicted the duration of the subsequent target disappearance. We propose that the transformation of the perceptual change into a report triggers a top-down mechanism that stabilizes the newly selected perceptual interpretation.
Asunto(s)
Ilusiones Ópticas , Corteza Visual/fisiología , Adulto , Ritmo beta , Femenino , Humanos , MasculinoRESUMEN
Changes in pupil size at constant light levels reflect the activity of neuromodulatory brainstem centers that control global brain state. These endogenously driven pupil dynamics can be synchronized with cognitive acts. For example, the pupil dilates during the spontaneous switches of perception of a constant sensory input in bistable perceptual illusions. It is unknown whether this pupil dilation only indicates the occurrence of perceptual switches, or also their content. Here, we measured pupil diameter in human subjects reporting the subjective disappearance and re-appearance of a physically constant visual target surrounded by a moving pattern ('motion-induced blindness' illusion). We show that the pupil dilates during the perceptual switches in the illusion and a stimulus-evoked 'replay' of that illusion. Critically, the switch-related pupil dilation encodes perceptual content, with larger amplitude for disappearance than re-appearance. This difference in pupil response amplitude enables prediction of the type of report (disappearance vs. re-appearance) on individual switches (receiver-operating characteristic: 61%). The amplitude difference is independent of the relative durations of target-visible and target-invisible intervals and subjects' overt behavioral report of the perceptual switches. Further, we show that pupil dilation during the replay also scales with the level of surprise about the timing of switches, but there is no evidence for an interaction between the effects of surprise and perceptual content on the pupil response. Taken together, our results suggest that pupil-linked brain systems track both the content of, and surprise about, perceptual events.
Asunto(s)
Percepción de Movimiento/fisiología , Pupila/fisiología , Percepción Visual/fisiología , Adulto , Femenino , Humanos , Masculino , Persona de Mediana Edad , Adulto JovenRESUMEN
While viewing certain stimuli, perception changes spontaneously in the face of constant input. For example, during "motion-induced blindness" (MIB), a small salient target spontaneously disappears and reappears when surrounded by a moving mask. Models of such bistable perceptual phenomena posit spontaneous fluctuations in neuronal activity throughout multiple stages of the visual cortical hierarchy. We used fMRI to link correlated activity fluctuations across human visual cortical areas V1 through V4 to the dynamics (rate and duration) of MIB target disappearance. We computed the correlations between the time series of fMRI activity in multiple retinotopic subregions corresponding to MIB target and mask. Linear decomposition of the matrix of temporal correlations revealed spatial patterns of activity fluctuations, regardless of whether or not these were time-locked to behavioral reports of target disappearance. The spatial pattern that dominated the activity fluctuations during MIB was spatially nonspecific, shared by all subregions, but did not reflect the dynamics of perception. By contrast, the fluctuations associated with the rate of MIB disappearance were retinotopically specific for the target subregion in V4, and the fluctuations associated with the duration of MIB disappearance states were target-specific in V1. Target-specific fluctuations in V1 have not previously been identified by averaging activity time-locked to behavioral reports of MIB disappearance. Our results suggest that different levels of the visual cortical hierarchy shape the dynamics of perception via distinct mechanisms, which are evident in distinct spatial patterns of spontaneous cortical activity fluctuations.
Asunto(s)
Percepción de Movimiento/fisiología , Corteza Visual/fisiología , Percepción Visual/fisiología , Adulto , Mapeo Encefálico , Femenino , Humanos , Imagen por Resonancia Magnética , Masculino , Movimiento (Física) , Ilusiones Ópticas/fisiología , Estimulación LuminosaRESUMEN
When perceptual decisions are coupled to a specific effector, preparatory motor cortical activity may provide a window into the dynamics of the perceptual choice. Specifically, previous studies have observed a buildup of choice-selective activity in motor regions over time reflecting the integrated sensory evidence provided by visual cortex. Here we ask how this choice-selective motor activity is modified by prior expectation during a visual motion discrimination task. Computational models of decision making formalize decisions as the accumulation of evidence from a starting point to a decision bound. Within this framework, expectation could change the starting point, rate of accumulation, or the decision bound. Using magneto-encephalography in human observers, we specifically tested for changes in the starting point in choice-selective oscillatory activity over motor cortex. Inducing prior expectation about motion direction biased subjects' perceptual judgments as well as the choice-selective motor activity in the 8-30 Hz frequency range before stimulus onset; the individual strength of these behavioral and neural biases were correlated across subjects. In the absence of explicit expectation cues, spontaneous biases in choice-selective activity were evident over motor cortex. These also predicted eventual perceptual choice and were, at least in part, induced by the choice on the previous trial. We conclude that both endogenous and explicitly induced perceptual expectations bias the starting point of decision-related activity, before the accumulation of sensory evidence.
Asunto(s)
Mapeo Encefálico , Conducta de Elección/fisiología , Percepción de Movimiento/fisiología , Corteza Motora/fisiología , Adulto , Señales (Psicología) , Femenino , Humanos , Magnetoencefalografía , MasculinoRESUMEN
Decision-makers often process new evidence selectively, depending on their current beliefs about the world. We asked whether such confirmation biases result from biases in the encoding of sensory evidence in the brain, or alternatively in the utilization of encoded evidence for behavior. Human participants estimated the source of a sequence of visual-spatial evidence samples while we measured cortical population activity with magnetoencephalography (MEG). Halfway through the sequence, participants were prompted to judge the more likely source category. Their processing of subsequent evidence depended on its consistency with the previously chosen category, but the encoding of evidence in cortical activity did not. Instead, the encoded evidence in parietal and primary visual cortex contributed less to the estimation report when that evidence was inconsistent with the previous choice. We conclude that confirmation bias originates from the way in which decision-makers utilize information encoded in the brain. This provides room for deliberative control.