Jose L. Pardo-Vazquez

Neural Correlates of Decisions and Their Outcomes in the Ventral Premotor Cortex

Selection of the appropriate action in a changing environment involves a chain of events that goes from perception through decision to action and evaluation of the outcomes. What and where in the brain are the correlates of these events? The ventral premotor cortex (PMv) is a candidate because (1) it is involved in sensory transformations for visually guided actions and in perceptual decisions, and (2) it is connected with sensory, motor, and high-level cognitive areas related to performance monitoring. Therefore, we hypothesized that it would be the site for representing sensory perception for action and for evaluating the decision consequences. Trained monkeys were required to discriminate the orientation of two lines showed in sequence and separated by a delay. Monkeys compared the orientation of the second line with the memory trace of the first and communicated whether the second was to the left or to the right of the first. Here we show that the activity of PMv neurons reflected (1) the first stimuli and its memory trace during the delay and comparison periods, (2) its comparison with the second stimuli, including the strength of the evidence, and (3) the result of the discrimination (choice). After the monkeys reported the choice, there were neurons that only encoded the choices, others only the outcomes, and others the choices and outcomes together. The representation of task cues, decision variables, and their outcomes suggest a role of PMv as part of a supervisory network involved in shaping future behavior and in learning.

A role for the ventral premotor cortex beyond performance monitoring

Depending on the circumstances, decision making requires either comparing current sensory information with that showed recently or with that recovered from long-term memory (LTM). In both cases, to learn from past decisions and adapt future ones, memories and outcomes have to be available after the report of a decision. The ventral premotor cortex (PMv) is a good candidate for integrating memory traces and outcomes because it is involved in working-memory, decision-making, and encoding the outcomes. To test this hypothesis we recorded the extracellular unit activity while monkeys performed 2 variants of a visual discrimination task. In one task, the decision was based on the comparison of the orientation of a current stimulus with that of another stimulus recently shown. In the other task, the monkeys had to compare the current orientation of the stimulus with the correct one retrieved from LTM. Here, we report that when the task required retrieval of the stimulus and its use in the following trials, the neurons continue encoding this internal representation together with the outcomes after the monkey has emitted the motor response. However, this codification did not occur when the stimulus was shown recently and updated every trial. These results suggest that the PMv activity represents the information needed to evaluate the consequences of a decision. We interpret these results as evidence that the PMv plays a role in evaluating the outcomes that can serve to learn and thus adapt future decision to environmental demands.

Optimizing the temporal dynamics of light to human perception

No previous research has tuned the temporal characteristics of light-emitting devices to enhance brightness perception in human vision, despite the potential for significant power savings. The role of stimulus duration on perceived contrast is unclear, due to contradiction between the models proposed by Bloch and by Broca and Sulzer over 100 years ago. We propose that the discrepancy is accounted for by the observer’s “inherent expertise bias,” a type of experimental bias in which the observer’s life-long experience with interpreting the sensory world overcomes perceptual ambiguities and biases experimental outcomes. By controlling for this and all other known biases, we show that perceived contrast peaks at durations of 50–100 ms, and we conclude that the Broca–Sulzer effect best describes human temporal vision. We also show that the plateau in perceived brightness with stimulus duration, described by Bloch’s law, is a previously uncharacterized type of temporal brightness constancy that, like classical constancy effects, serves to enhance object recognition across varied lighting conditions in natural vision—although this is a constancy effect that normalizes perception across temporal modulation conditions. A practical outcome of this study is that tuning light-emitting devices to match the temporal dynamics of the human visual system’s temporal response function will result in significant power savings.

Decision-Making, Behavioral Supervision and Learning: An Executive Role for the Ventral Premotor Cortex?

In order to adjust the behavioral performance in a changing environment, subjects have to monitor their evolving actions and to know whether their responses were correct or incorrect. This requires self-awareness, cognitive flexibility, working memory (WM), and decision making that frequently are impaired in psychosis. What is the neural substrate of these processes and where are these substrates located? Dysfunction of prefrontal, parietal, temporal cortices, and associated subcortical structures are known to be involved in some of these symptoms. The prefrontal–subcortical circuits have been the main focus of study while other cortical areas such as the premotor cortex have received less attention. The main focus of this review is about the evidence that the ventral premotor cortex processes both recent sensory information and that from long-term memory to decide and evaluate the behavior of previous decisions. This process may serve for learning and thus adapting future behavior to environmental demands. Therefore, dysfunction of this cortical area could be related to some cognitive neuropsychiatric disorders.

External validation of the computerized, group administrable adaptation of the “operation span task”

One of the most widely used tasks for measuring working memory capacity is the operation span task (OSPAN; Turner & Engle, 1989). This task has almost always been applied individually, and stimuli presentation is controlled by the experimenter. Recently, De Neys, d’Ydewalle, Schaeken, and Vos (2002) improved the administration procedure by designing an automated, group-administrable version of the task (GOSPAN). They found GOSPAN to be reliable, and they also provided evidence on its validity (a significant positive correlation between GOSPAN and OSPAN scores). However, an external test of GOSPAN validity is still lacking. In this work, we present such a validation for the automated version, when the task is administered both individually (Experiment 1) and to groups (Experiment 2). There are abundant previous data on the relation between working memory capacity and reading comprehension. In this work, this relation is studied using an automated OSPAN version to measure working memory capacity. Given that our results are similar to those found using the original OSPAN, our data support the external validity of the automated version of the task. We also tested the reliability of the task and found high internal consistency in both experiments.

Decision-Making in the Ventral Premotor Cortex Harbinger of Action

Although the premotor (PM) cortex was once viewed as the substrate of pure motor functions, soon it was realized that it was involved in higher brain functions. By this it is meant that the PM cortex functions would better be explained as motor set, preparation for limb movement, or sensory guidance of movement rather than solely by a fixed link to motor performance. These findings, together with a better knowledge of the PM cortex histology and hodology in human and non-human primates prompted quantitative studies of this area combining behavioral tasks with electrophysiological recordings. In addition, the exploration of the PM cortex neurons with qualitative methods also suggested its participation in higher functions. Behavioral choices frequently depend on temporal cues, which together with knowledge of previous outcomes and expectancies are combined to decide and choose a behavioral action. In decision-making the knowledge about the consequences of decisions, either correct or incorrect, is fundamental because they can be used to adapt future behavior. The neuronal correlates of a decision process have been described in several cortical areas of primates. Among them, there is evidence that the monkey ventral premotor (PMv) cortex, an anatomical and physiological well-differentiated area of the PM cortex, supports both perceptual decisions and performance monitoring. Here we review the evidence that the steps in a decision-making process are encoded in the firing rate of the PMv neurons. This provides compelling evidence suggesting that the PMv is involved in the use of recent and long-term sensory memory to decide, execute, and evaluate the outcomes of the subjects’ choices.

Ventral premotor cortex neuronal activity matches perceptual decisions

The relationship between neuronal activity and psychophysical judgments is central to understanding the brain mechanisms responsible for perceptual decisions. The ventral premotor cortex is known to be involved in representing different components of the decision‐making process. In this cortical area, however, neither the neuronal ability to discriminate nor the trial‐to‐trial relationship between neuronal activity and behavior have been studied during visual decision‐making. We recorded from single neurons while monkeys reported a decision based on the comparison of the orientation of two lines shown sequentially and separated by a delay. Analyses based on signal detection theory provided both the behavioral and neuronal sensitivities (d′) and the coherence between behavioral and neuronal choices. To determine the temporal evolution of neuronal sensitivity and of coherence, the optimal size and position of the encoding windows were assessed. For a subset of neurons from the premotor ventral cortex, neuronal sensitivity was close to behavioral sensitivity and the trial‐to‐trial coherence between the neuronal and behavioral choices was close to 100%. By comparing these results with those obtained in a motor control task we ruled out the possibility of this activity being explained by the motor component of the task. These results suggest that activity in the ventral premotor cortex explains behavioral performance and predicts trial‐to‐trial subject choices.

Deletion of the cold thermoreceptor TRPM8 increases heat loss and food intake leading to reduced body temperature and obesity in mice.

The coupling of energy homeostasis to thermoregulation is essential to maintain homeothermy in changing external environments. We studied the role of the cold thermoreceptor TRPM8 in this interplay in mice of both sexes. We demonstrate that TRPM8 is required for a precise thermoregulation in response to cold, in fed and fasting. Trpm8−/− mice exhibited a fall of 0.7°C in core body temperature when housed at cold temperatures, and a deep hypothermia (<30°C) during food deprivation. In both situations, TRPM8 deficiency induced an increase in tail heat loss. This, together with the presence of TRPM8-sensory fibers innervating the main tail vessels, unveils a major role of this ion channel in tail vasomotor regulation. Finally, TRPM8 deficiency had a remarkable impact on energy balance. Trpm8−/− mice raised at mild cold temperatures developed late-onset obesity and metabolic dysfunction, with daytime hyperphagia and reduction of fat oxidation as plausible causal factors. In conclusion, TRPM8 fine-tunes eating behavior and fuel utilization during thermoregulatory adjustments to mild cold. Persistent imbalances in these responses result in obesity. SIGNIFICANCE STATEMENT The thermosensitive ion channel TRPM8 is required for a precise thermoregulatory response to cold and fasting, playing an important role in tail vasoconstriction, and therefore heat conservation, as well as in the regulation of ingestive behavior and metabolic fuel selection upon cooling. Indeed, TRPM8-deficient mice, housed in a mild cold environment, displayed an increase in tail heat loss and lower core body temperature, associated with the development of late-onset obesity with glucose and lipid metabolic dysfunction. A persistent diurnal hyperphagia and reduced fat oxidation constitute plausible underlying mechanisms in the background of a deficient thermoregulatory adjustment to mild cold ambient temperatures.

EEG activity represents the correctness of perceptual decisions trial-by-trial

Performance monitoring is an executive function, which we depend on for detecting and evaluating the consequences of our behavior. Although event related potentials (ERPs) have revealed the existence of differences after correct and incorrect decisions, it is not known whether there is a trial-by-trial representation of the accuracy of the decision. We recorded the electroencephalographic activity (EEG) while participants performed a perceptual discrimination task, with two levels of difficulty, in which they received immediate feedback. Receiver Operating Characteristic (ROC) analyses were used to reveal two components that convey trial-by-trial representations of the correctness of the decisions. Firstly, the performance monitoring-related negativity (PM-N), a negative deflection whose amplitude is higher (more negative) after incorrect trials. Secondly, the performance monitoring-related positivity (PM-P), a positive deflection whose amplitude is higher after incorrect trials. During the time periods corresponding to these components, trials can be accurately categorized as correct or incorrect by looking at the EEG activity; this categorization is more accurate when based on the PM-P. We further show that the difficulty of the discrimination task has a different effect on each component: after easy trials the latency of the PM-N is shorter and the amplitude of the PM-P is higher than after difficult trials. Consistent with previous interpretations of performance-related ERPs, these results suggest a functional differentiation between these components. The PM-N could be related to an automatic error detection system, responsible for fast behavioral corrections of ongoing actions, while the PM-P could reflect the difference between expected and actual outcomes and be related to long-term changes in the decision process.

Assessing neural activity related to decision-making through flexible odds ratio curves and their derivatives.

It is well established that neural activity is stochastically modulated over time. Therefore, direct comparisons across experimental conditions and determination of change points or maximum firing rates are not straightforward. This study sought to compare temporal firing probability curves that may vary across groups defined by different experimental conditions. Odds-ratio (OR) curves were used as a measure of comparison, and the main goal was to provide a global test to detect significant differences of such curves through the study of their derivatives. An algorithm is proposed that enables ORs based on generalized additive models, including factor-by-curve-type interactions to be flexibly estimated. Bootstrap methods were used to draw inferences from the derivatives curves, and binning techniques were applied to speed up computation in the estimation and testing processes. A simulation study was conducted to assess the validity of these bootstrap-based tests. This methodology was applied to study premotor ventral cortex neural activity associated with decision-making. The proposed statistical procedures proved very useful in revealing the neural activity correlates of decision-making in a visual discrimination task.