Toward a neuroscience of natural behavior.

One of the most exciting new developments in systems neuroscience is the progress being made toward neurophysiological experiments that move beyond simplified laboratory settings and address the richness of natural behavior. This is enabled by technological advances such as wireless recording in freely moving animals, automated quantification of behavior, and new methods for analyzing large data sets. Beyond new empirical methods and data, however, there is also a need for new theories and concepts to interpret that data. Such theories need to address the particular challenges of natural behavior, which often differ significantly from the scenarios studied in traditional laboratory settings. Here, we discuss some strategies for developing such novel theories and concepts and some example hypotheses being proposed.

Generating meaning: active inference and the scope and limits of passive AI.

Prominent accounts of sentient behavior depict brains as generative models of organismic interaction with the world, evincing intriguing similarities with current advances in generative artificial intelligence (AI). However, because they contend with the control of purposive, life-sustaining sensorimotor interactions, the generative models of living organisms are inextricably anchored to the body and world. Unlike the passive models learned by generative AI systems, they must capture and control the sensory consequences of action. This allows embodied agents to intervene upon their worlds in ways that constantly put their best models to the test, thus providing a solid bedrock that is - we argue - essential to the development of genuine understanding. We review the resulting implications and consider future directions for generative AI.

Parallel processing of value-related information during multi-attribute decisions.

When choosing between options with multiple attributes, do we integrate all attributes into a unified measure for comparison, or does the comparison also occur at the level of each attribute, involving parallel processes that can dynamically influence each other? What happens when independent sensory features all carry information about the same decision factor, such as reward value? To investigate these questions, we asked human participants to perform a two-alternative forced choice reaching task in which the reward value of a target was indicated by two visual attributes-its brightness ("bottom-up," BU feature) and its orientation ("top-down," TD feature). If decisions always occur after the integration of both features, there should be no difference in the reaction time (RT) regardless of the attribute combinations that drove the choice. Counter to that prediction, RT distributions depended on the attribute combinations of given targets and the choices made by participants. RTs were shortest when both attributes were congruent or when the choice was based on the bottom-up feature, and longer when the attributes were in conflict (favoring opposite options). In conflict trials, nearly two-thirds of participants made faster decisions when choosing the option favored by the bottom-up feature than when choosing the top-down-favored option. We also observed mid-reach changes-of-mind in a subset of conflict trials, mostly changing from the bottom-up to the top-down-favored target. These data suggest that multi-attribute value-based decisions are better explained by a distributed process including competition among different features than by a competition based on a single, integrated estimate of value.NEW & NOTEWORTHY We show that during value-based decisions, humans do not always use all reward-related information to make their choice, but instead can "jump the gun" using partial information. In particular, when different sources of information were in conflict, early decisions were mostly based on fast bottom-up information, and sometimes followed by corrective changes-of-mind based on slower top-down information. This supports parallel decision processes among different information sources, as opposed to a single integrated "common currency."

Beyond simple laboratory studies: Developing sophisticated models to study rich behavior.

Psychology and neuroscience are concerned with the study of behavior, of internal cognitive processes, and their neural foundations. However, most laboratory studies use constrained experimental settings that greatly limit the range of behaviors that can be expressed. While focusing on restricted settings ensures methodological control, it risks impoverishing the object of study: by restricting behavior, we might miss key aspects of cognitive and neural functions. In this article, we argue that psychology and neuroscience should increasingly adopt innovative experimental designs, measurement methods, analysis techniques and sophisticated computational models to probe rich, ecologically valid forms of behavior, including social behavior. We discuss the challenges of studying rich forms of behavior as well as the novel opportunities offered by state-of-the-art methodologies and new sensing technologies, and we highlight the importance of developing sophisticated formal models. We exemplify our arguments by reviewing some recent streams of research in psychology, neuroscience and other fields (e.g., sports analytics, ethology and robotics) that have addressed rich forms of behavior in a model-based manner. We hope that these "success cases" will encourage psychologists and neuroscientists to extend their toolbox of techniques with sophisticated behavioral models - and to use them to study rich forms of behavior as well as the cognitive and neural processes that they engage.

Integrated neural dynamics of sensorimotor decisions and actions.

Recent theoretical models suggest that deciding about actions and executing them are not implemented by completely distinct neural mechanisms but are instead two modes of an integrated dynamical system. Here, we investigate this proposal by examining how neural activity unfolds during a dynamic decision-making task within the high-dimensional space defined by the activity of cells in monkey dorsal premotor (PMd), primary motor (M1), and dorsolateral prefrontal cortex (dlPFC) as well as the external and internal segments of the globus pallidus (GPe, GPi). Dimensionality reduction shows that the four strongest components of neural activity are functionally interpretable, reflecting a state transition between deliberation and commitment, the transformation of sensory evidence into a choice, and the baseline and slope of the rising urgency to decide. Analysis of the contribution of each population to these components shows meaningful differences between regions but no distinct clusters within each region, consistent with an integrated dynamical system. During deliberation, cortical activity unfolds on a two-dimensional "decision manifold" defined by sensory evidence and urgency and falls off this manifold at the moment of commitment into a choice-dependent trajectory leading to movement initiation. The structure of the manifold varies between regions: In PMd, it is curved; in M1, it is nearly perfectly flat; and in dlPFC, it is almost entirely confined to the sensory evidence dimension. In contrast, pallidal activity during deliberation is primarily defined by urgency. We suggest that these findings reveal the distinct functional contributions of different brain regions to an integrated dynamical system governing action selection and execution.

Performance-gated deliberation: A context-adapted strategy in which urgency is opportunity cost.

Finding the right amount of deliberation, between insufficient and excessive, is a hard decision making problem that depends on the value we place on our time. Average-reward, putatively encoded by tonic dopamine, serves in existing reinforcement learning theory as the opportunity cost of time, including deliberation time. Importantly, this cost can itself vary with the environmental context and is not trivial to estimate. Here, we propose how the opportunity cost of deliberation can be estimated adaptively on multiple timescales to account for non-stationary contextual factors. We use it in a simple decision-making heuristic based on average-reward reinforcement learning (AR-RL) that we call Performance-Gated Deliberation (PGD). We propose PGD as a strategy used by animals wherein deliberation cost is implemented directly as urgency, a previously characterized neural signal effectively controlling the speed of the decision-making process. We show PGD outperforms AR-RL solutions in explaining behaviour and urgency of non-human primates in a context-varying random walk prediction task and is consistent with relative performance and urgency in a context-varying random dot motion task. We make readily testable predictions for both neural activity and behaviour.

Hasty sensorimotor decisions rely on an overlap of broad and selective changes in motor activity.

Humans and other animals are able to adjust their speed-accuracy trade-off (SAT) at will depending on the urge to act, favoring either cautious or hasty decision policies in different contexts. An emerging view is that SAT regulation relies on influences exerting broad changes on the motor system, tuning its activity up globally when hastiness is at premium. The present study aimed to test this hypothesis. A total of 50 participants performed a task involving choices between left and right index fingers, in which incorrect choices led either to a high or to a low penalty in 2 contexts, inciting them to emphasize either cautious or hasty policies. We applied transcranial magnetic stimulation (TMS) on multiple motor representations, eliciting motor-evoked potentials (MEPs) in 9 finger and leg muscles. MEP amplitudes allowed us to probe activity changes in the corresponding finger and leg representations, while participants were deliberating about which index to choose. Our data indicate that hastiness entails a broad amplification of motor activity, although this amplification was limited to the chosen side. On top of this effect, we identified a local suppression of motor activity, surrounding the chosen index representation. Hence, a decision policy favoring speed over accuracy appears to rely on overlapping processes producing a broad (but not global) amplification and a surround suppression of motor activity. The latter effect may help to increase the signal-to-noise ratio of the chosen representation, as supported by single-trial correlation analyses indicating a stronger differentiation of activity changes in finger representations in the hasty context.

Shared population-level dynamics in monkey premotor cortex during solo action, joint action and action observation.

Studies of neural population dynamics of cell activity from monkey motor areas during reaching show that it mostly represents the generation and timing of motor behavior. We compared neural dynamics in dorsal premotor cortex (PMd) during the performance of a visuomotor task executed individually or cooperatively and during an observation task. In the visuomotor conditions, monkeys applied isometric forces on a joystick to guide a visual cursor in different directions, either alone or jointly with a conspecific. In the observation condition, they observed the cursor's motion guided by the partner. We found that in PMd neural dynamics were widely shared across action execution and observation, with cursor motion directions more accurately discriminated than task types. This suggests that PMd encodes spatial aspects irrespective of specific behavioral demands. Furthermore, our results suggest that largest components of premotor population dynamics, which have previously been suggested to reflect a transformation from planning to movement execution, may rather reflect higher cognitive-motor processes, such as the covert representation of actions and goals shared across tasks that require movement and those that do not.

Neuroscience needs evolution.

The nervous system is a product of evolution. That is, it was constructed through a long series of modifications, within the strong constraints of heredity, and continuously subjected to intense selection pressures. As a result, the organization and functions of the brain are shaped by its history. We believe that this fact, underappreciated in contemporary systems neuroscience, offers an invaluable aid for helping us resolve the brain's mysteries. Indeed, we think that the consideration of evolutionary history ought to take its place alongside other intellectual tools used to understand the brain, such as behavioural experiments, studies of anatomical structure and functional characterization based on recordings of neural activity. In this introduction, we argue for the importance of evolution by highlighting specific examples of ways that evolutionary theory can enhance neuroscience. The rest of the theme issue elaborates this point, emphasizing the conservative nature of neural evolution, the important consequences of specific transitions that occurred in our history, and the ways in which considerations of evolution can shed light on issues ranging from specific mechanisms to fundamental principles of brain organization. This article is part of the theme issue 'Systems neuroscience through the lens of evolutionary theory'.

Evolution of behavioural control from chordates to primates.

This article outlines a hypothetical sequence of evolutionary innovations, along the lineage that produced humans, which extended behavioural control from simple feedback loops to sophisticated control of diverse species-typical actions. I begin with basic feedback mechanisms of ancient mobile animals and follow the major niche transitions from aquatic to terrestrial life, the retreat into nocturnality in early mammals, the transition to arboreal life and the return to diurnality. Along the way, I propose a sequence of elaboration and diversification of the behavioural repertoire and associated neuroanatomical substrates. This includes midbrain control of approach versus escape actions, telencephalic control of local versus long-range foraging, detection of affordances by the dorsal pallium, diversified control of nocturnal foraging in the mammalian neocortex and expansion of primate frontal, temporal and parietal cortex to support a wide variety of primate-specific behavioural strategies. The result is a proposed functional architecture consisting of parallel control systems, each dedicated to specifying the affordances for guiding particular species-typical actions, which compete against each other through a hierarchy of selection mechanisms. This article is part of the theme issue 'Systems neuroscience through the lens of evolutionary theory'.

Changes of Mind after Movement Onset Depend on the State of the Motor System.

Decision-making is traditionally described as a cognitive process of deliberation followed by commitment to an action choice, preceding the planning and execution of the chosen action. However, this is challenged by recent data suggesting that during situated decisions, multiple options are specified simultaneously and compete in premotor cortical areas for selection and execution. Previous studies focused on the competition during planning and left unaddressed the dynamics of decisions during movement. Does deliberation extend into the execution phase? Are nonselected options still considered? Here we studied a decision-making task in which human participants were instructed to select a reaching path trajectory from an origin to a rectangular target, where reward was distributed nonuniformly at the target. Critically, we applied mechanical perturbations to the arm during movement to study under which conditions such perturbations produce changes of mind. Our results show that participants initially selected the direction of movement toward the highest reward region and changed their mind most frequently when the two choices offered the same reward, showing that deliberation continues and follows cost-benefit considerations during movement. Furthermore, changes of mind were dependent on the intensity of the perturbation and the current state of the motor system, including velocity and distance to targets. Although reward remains most relevant, our results indicate that the state of the motor system when the perturbation occurs is a crucial determinant of changes of mind.

The road towards understanding embodied decisions.

Most current decision-making research focuses on classical economic scenarios, where choice offers are prespecified and where action dynamics play no role in the decision. However, our brains evolved to deal with different choice situations: "embodied decisions". As examples of embodied decisions, consider a lion that has to decide which gazelle to chase in the savannah or a person who has to select the next stone to jump on when crossing a river. Embodied decision settings raise novel questions, such as how people select from time-varying choice options and how they track the most relevant choice attributes; but they have long remained challenging to study empirically. Here, we summarize recent progress in the study of embodied decisions in sports analytics and experimental psychology. Furthermore, we introduce a formal methodology to identify the relevant dimensions of embodied choices (present and future affordances) and to map them into the attributes of classical economic decisions (probabilities and utilities), hence aligning them. Studying embodied decisions will greatly expand our understanding of what decision-making is.

Trading accuracy for speed over the course of a decision.

Humans and other animals often need to balance the desire to gather sensory information (to make the best choice) with the urgency to act, facing a speed-accuracy tradeoff (SAT). Given the ubiquity of SAT across species, extensive research has been devoted to understanding the computational mechanisms allowing its regulation at different timescales, including from one context to another, and from one decision to another. However, animals must frequently change their SAT on even shorter timescales-that is, over the course of an ongoing decision-and little is known about the mechanisms that allow such rapid adaptations. The present study aimed at addressing this issue. Human subjects performed a decision task with changing evidence. In this task, subjects received rewards for correct answers but incurred penalties for mistakes. An increase or a decrease in penalty occurring halfway through the trial promoted rapid SAT shifts, favoring speeded decisions either in the early or in the late stage of the trial. Importantly, these shifts were associated with stage-specific adjustments in the accuracy criterion exploited for committing to a choice. Those subjects who decreased the most their accuracy criterion at a given decision stage exhibited the highest gain in speed, but also the highest cost in terms of performance accuracy at that time. Altogether, the current findings offer a unique extension of previous work, by suggesting that dynamic cha*nges in accuracy criterion allow the regulation of the SAT within the timescale of a single decision.NEW & NOTEWORTHY Extensive research has been devoted to understanding the mechanisms allowing the regulation of the speed-accuracy tradeoff (SAT) from one context to another and from one decision to another. Here, we show that humans can voluntarily change their SAT on even shorter timescales-that is, over the course of a decision. These rapid SAT shifts are associated with dynamic adjustments in the accuracy criterion exploited for committing to a choice.

Evidence and Urgency Related EEG Signals during Dynamic Decision-Making in Humans.

A successful class of models link decision-making to brain signals by assuming that evidence accumulates to a decision threshold. These evidence accumulation models have identified neuronal activity that appears to reflect sensory evidence and decision variables that drive behavior. More recently, an additional evidence-independent and time-variant signal, called urgency, has been hypothesized to accelerate decisions in the face of insufficient evidence. However, most decision-making paradigms tested with fMRI or EEG in humans have not been designed to disentangle evidence accumulation from urgency. Here we use a face-morphing decision-making task in combination with EEG and a hierarchical Bayesian model to identify neural signals related to sensory and decision variables, and to test the urgency-gating model. Forty females and 34 males took part (mean age, 23.4 years). We find that an evoked potential time locked to the decision, the centroparietal positivity, reflects the decision variable from the computational model. We further show that the unfolding of this signal throughout the decision process best reflects the product of sensory evidence and an evidence-independent urgency signal. Urgency varied across subjects, suggesting that it may represent an individual trait. Our results show that it is possible to use EEG to distinguish neural signals related to sensory evidence accumulation, decision variables, and urgency. These mechanisms expose principles of cognitive function in general and may have applications to the study of pathologic decision-making such as in impulse control and addictive disorders.SIGNIFICANCE STATEMENT Perceptual decisions are often described by a class of models that assumes that sensory evidence accumulates gradually over time until a decision threshold is reached. In the present study, we demonstrate that an additional urgency signal impacts how decisions are formed. This endogenous signal encourages one to respond as time elapses. We found that neural decision signals measured by EEG reflect the product of sensory evidence and an evidence-independent urgency signal. A nuanced understanding of human decisions, and the neural mechanisms that support it, can improve decision-making in many situations and potentially ameliorate dysfunction when it has gone awry.

Reaching decisions during ongoing movements.

Neurophysiological studies suggest that when decisions are made between concrete actions, the selection process involves a competition between potential action representations in the same sensorimotor structures involved in executing those actions. However, it is unclear how such models can explain situations, often encountered during natural behavior, in which we make decisions while were are already engaged in performing an action. Does the process of deliberation characterized in classical studies of decision-making proceed the same way when subjects are deciding while already acting? In the present study, human subjects continuously tracked a target moving in the horizontal plane and were occasionally presented with a new target to which they could freely choose to switch at any time, whereupon it became the new tracked target. We found that the probability of choosing to switch increased with decreasing distance to the new target and increasing size of the new target relative to the tracked target, as well as when the direction to the new target was aligned (either toward or opposite) to the current tracking direction. However, contrary to our expectations, subjects did not choose targets that minimized the energetic costs of execution, as calculated by a biomechanical model of the arm. When the constraints of continuous tracking were removed in variants of the task involving point-to-point movements, the expected preference for lower cost choices was seen. These results are discussed in the context of current theories of nested feedback control, internal models of forward dynamics, and high-dimensional neural spaces.NEW & NOTEWORTHY Current theories of decision-making primarily address how subjects make decisions before executing selected actions. However, in our daily lives we often make decisions while already performing some action (e.g., while playing a sport or navigating through a crowd). To gain insight into how current theories can be extended to such "decide-while-acting" scenarios, we examined human decisions during continuous manual tracking and found some intriguing departures from how decisions are made in classical "decide-then-act" paradigms.

Microstimulation of dorsal premotor and primary motor cortex delays the volitional commitment to an action choice.

Humans and other animals are faced with decisions about actions on a daily basis. These typically include a period of deliberation that ends with the commitment to a choice, which then leads to the overt expression of that choice through action. Previous studies with monkeys have demonstrated that neural activity in sensorimotor areas correlates with the deliberation process and reflects the moment of commitment before movement initiation, but the causal roles of these regions are challenging to establish. Here, we tested whether dorsal premotor (PMd) and primary motor cortex (M1) are causally involved in the volitional commitment to a reaching choice. We found that brief subthreshold microstimulation in PMd or M1 delayed commitment to an action but not the initiation of the action itself. Importantly, microstimulation only had a significant effect when it was delivered close to and before commitment time. These results are consistent with the proposal that PMd and M1 participate in the commitment process, which occurs when a critical firing rate difference is reached between cells voting for the selected option and those voting for the competing one.NEW & NOTEWORTHY The neural substrates of decisions between actions are typically investigated by correlating neural activity and subjects' decision behavior, but this does not establish causality. In a reaching decision task, we demonstrate that subthreshold microstimulation of the monkey dorsal premotor cortex or primary motor cortex delays the deliberation duration if applied shortly before choice commitment. This result suggests a causal role of the sensorimotor cortex in the determination of decisions between actions.

A sensorimotor alternative to coding is possible.

If we abandon the coding metaphor in favor of models of the full behavioral loop, we need a way to dissect that loop into understandable pieces. I suggest that evolutionary data provide a solution. We can subdivide behavior into parallel sensorimotor subsystems by following the phylogenetic history of how those systems differentiated and specialized during our evolution, leading to promising ways of re-interpreting neural activity within the context of its pragmatic role in mediating interaction.

No one knows what attention is.

In this article, we challenge the usefulness of "attention" as a unitary construct and/or neural system. We point out that the concept has too many meanings to justify a single term, and that "attention" is used to refer to both the explanandum (the set of phenomena in need of explanation) and the explanans (the set of processes doing the explaining). To illustrate these points, we focus our discussion on visual selective attention. It is argued that selectivity in processing has emerged through evolution as a design feature of a complex multi-channel sensorimotor system, which generates selective phenomena of "attention" as one of many by-products. Instead of the traditional analytic approach to attention, we suggest a synthetic approach that starts with well-understood mechanisms that do not need to be dedicated to attention, and yet account for the selectivity phenomena under investigation. We conclude that what would serve scientific progress best would be to drop the term "attention" as a label for a specific functional or neural system and instead focus on behaviorally relevant selection processes and the many systems that implement them.

Motor cortex disruption delays motor processes but not deliberation about action choices.

Decisions about actions typically involve a period of deliberation that ends with the commitment to a choice and the motor processes overtly expressing that choice. Previous studies have shown that neural activity in sensorimotor areas, including the primary motor cortex (M1), correlates with deliberation features during action selection. However, the causal contribution of these areas to the decision process remains unclear. Here, we investigated whether M1 determines choice commitment or whether it simply reflects decision signals coming from upstream structures and instead mainly contributes to the motor processes that follow commitment. To do so, we tested the impact of a disruption of M1 activity, induced by continuous theta burst stimulation (cTBS), on the behavior of human subjects in 1) a simple reaction time (SRT) task allowing us to estimate the duration of the motor processes and 2) a modified version of the tokens task (Cisek P, Puskas GA, El-Murr S. J Neurosci 29: 11560-11571, 2009), which allowed us to estimate subjects' time of commitment as well as accuracy criterion. The efficiency of cTBS was attested by a reduction in motor evoked potential amplitudes following M1 disruption compared with those following a sham stimulation. Furthermore, M1 cTBS lengthened SRTs, indicating that motor processes were perturbed by the intervention. Importantly, all of the behavioral results in the tokens task were similar following M1 disruption and sham stimulation, suggesting that the contribution of M1 to the deliberation process is potentially negligible. Taken together, these findings favor the view that M1 contribution is downstream of the decision process.NEW & NOTEWORTHY Decisions between actions are ubiquitous in the animal realm. Deliberation during action choices entails changes in the activity of the sensorimotor areas controlling those actions, but the causal role of these areas is still often debated. With the use of continuous theta burst stimulation, we show that disrupting the primary motor cortex (M1) delays the motor processes that follow instructed commitment but does not alter volitional deliberation, suggesting that M1 contribution may be downstream of the decision process.

Resynthesizing behavior through phylogenetic refinement.

This article proposes that biologically plausible theories of behavior can be constructed by following a method of "phylogenetic refinement," whereby they are progressively elaborated from simple to complex according to phylogenetic data on the sequence of changes that occurred over the course of evolution. It is argued that sufficient data exist to make this approach possible, and that the result can more effectively delineate the true biological categories of neurophysiological mechanisms than do approaches based on definitions of putative functions inherited from psychological traditions. As an example, the approach is used to sketch a theoretical framework of how basic feedback control of interaction with the world was elaborated during vertebrate evolution, to give rise to the functional architecture of the mammalian brain. The results provide a conceptual taxonomy of mechanisms that naturally map to neurophysiological and neuroanatomical data and that offer a context for defining putative functions that, it is argued, are better grounded in biology than are some of the traditional concepts of cognitive science.