Integrating costs and benefits is crucial for optimal decision-making. Although much is known about decisions that involve outcome-related costs (e.g., delay, risk), many of our choices are attached ...to actions and require an evaluation of the associated motor costs. Yet how the brain incorporates motor costs into choices remains largely unclear. We used human fMRI during choices involving monetary reward and physical effort to identify brain regions that serve as a choice comparator for effort-reward trade-offs. By independently varying both options' effort and reward levels, we were able to identify the neural signature of a comparator mechanism. A network involving supplementary motor area and the caudal portion of dorsal anterior cingulate cortex encoded the difference in reward (positively) and effort levels (negatively) between chosen and unchosen choice options. We next modeled effort-discounted subjective values using a novel behavioral model. This revealed that the same network of regions involving dorsal anterior cingulate cortex and supplementary motor area encoded the difference between the chosen and unchosen options' subjective values, and that activity was best described using a concave model of effort-discounting. In addition, this signal reflected how precisely value determined participants' choices. By contrast, separate signals in supplementary motor area and ventromedial prefrontal cortex correlated with participants' tendency to avoid effort and seek reward, respectively. This suggests that the critical neural signature of decision-making for choices involving motor costs is found in human cingulate cortex and not ventromedial prefrontal cortex as typically reported for outcome-based choice. Furthermore, distinct frontal circuits seem to drive behavior toward reward maximization and effort minimization.
The neural processes that govern the trade-off between expected benefits and motor costs remain largely unknown. This is striking because energetic requirements play an integral role in our day-to-day choices and instrumental behavior, and a diminished willingness to exert effort is a characteristic feature of a range of neurological disorders. We use a new behavioral characterization of how humans trade off reward maximization with effort minimization to examine the neural signatures that underpin such choices, using BOLD MRI neuroimaging data. We find the critical neural signature of decision-making, a signal that reflects the comparison of value between choice options, in human cingulate cortex, whereas two distinct brain circuits drive behavior toward reward maximization or effort minimization.
There has been considerable interest from the fields of biology, economics, psychology, and ecology about how decision costs decrease the value of rewarding outcomes. For example, formal descriptions ...of how reward value changes with increasing temporal delays allow for quantifying individual decision preferences, as in animal species populating different habitats, or normal and clinical human populations. Strikingly, it remains largely unclear how humans evaluate rewards when these are tied to energetic costs, despite the surge of interest in the neural basis of effort-guided decision-making and the prevalence of disorders showing a diminished willingness to exert effort (e.g., depression). One common assumption is that effort discounts reward in a similar way to delay. Here we challenge this assumption by formally comparing competing hypotheses about effort and delay discounting. We used a design specifically optimized to compare discounting behavior for both effort and delay over a wide range of decision costs (Experiment 1). We then additionally characterized the profile of effort discounting free of model assumptions (Experiment 2). Contrary to previous reports, in both experiments effort costs devalued reward in a manner opposite to delay, with small devaluations for lower efforts, and progressively larger devaluations for higher effort-levels (concave shape). Bayesian model comparison confirmed that delay-choices were best predicted by a hyperbolic model, with the largest reward devaluations occurring at shorter delays. In contrast, an altogether different relationship was observed for effort-choices, which were best described by a model of inverse sigmoidal shape that is initially concave. Our results provide a novel characterization of human effort discounting behavior and its first dissociation from delay discounting. This enables accurate modelling of cost-benefit decisions, a prerequisite for the investigation of the neural underpinnings of effort-guided choice and for understanding the deficits in clinical disorders characterized by behavioral inactivity.
The medial frontal cortex and adjacent orbitofrontal cortex have been the focus of investigations of decision-making, behavioral flexibility, and social behavior. We review studies conducted in ...humans, macaques, and rodents and argue that several regions with different functional roles can be identified in the dorsal anterior cingulate cortex, perigenual anterior cingulate cortex, anterior medial frontal cortex, ventromedial prefrontal cortex, and medial and lateral parts of the orbitofrontal cortex. There is increasing evidence that the manner in which these areas represent the value of the environment and specific choices is different from subcortical brain regions and more complex than previously thought. Although activity in some regions reflects distributions of reward and opportunities across the environment, in other cases, activity reflects the structural relationships between features of the environment that animals can use to infer what decision to take even if they have not encountered identical opportunities in the past.
The prefrontal cortex (PFC) provides high-level coordination of behavior but is not a homogeneous structure. In this review, Klein-Flügge et al. compare the function of several distinct PFC regions and connected subcortical nuclei in decision-making, behavioral flexibility, and social behavior.
Neural mechanisms that mediate the ability to make value-guided decisions have received substantial attention in humans and animals
. Experiments in animals typically involve long training periods. ...By contrast, choices in the real world often need to be made between new options spontaneously. It is therefore possible that the neural mechanisms targeted in animal studies differ from those required for new decisions, which are typical of human imaging studies. Here we show that the primate medial frontal cortex (MFC)
is involved in making new inferential choices when the options have not been previously experienced. Macaques spontaneously inferred the values of new options via similarities with the component parts of previously encountered options. Functional magnetic resonance imaging (fMRI) suggested that this ability was mediated by the MFC, which is rarely investigated in monkeys
; MFC activity reflected different processes of comparison for unfamiliar and familiar options. Multidimensional representations of options in the MFC used a coding scheme resembling that of grid cells, which is well known in spatial navigation
, to integrate dimensions in this non-physical space
during novel decision-making. By contrast, the orbitofrontal cortex held specific object-based value representations
. In addition, minimally invasive ultrasonic disruption
of MFC, but not adjacent tissue, altered the estimation of novel choice values.
To understand brain circuits it is necessary both to record and manipulate their activity. Transcranial ultrasound stimulation (TUS) is a promising non-invasive brain stimulation technique. To date, ...investigations report short-lived neuromodulatory effects, but to deliver on its full potential for research and therapy, ultrasound protocols are required that induce longer-lasting 'offline' changes. Here, we present a TUS protocol that modulates brain activation in macaques for more than one hour after 40 s of stimulation, while circumventing auditory confounds. Normally activity in brain areas reflects activity in interconnected regions but TUS caused stimulated areas to interact more selectively with the rest of the brain. In a within-subject design, we observe regionally specific TUS effects for two medial frontal brain regions - supplementary motor area and frontal polar cortex. Independently of these site-specific effects, TUS also induced signal changes in the meningeal compartment. TUS effects were temporary and not associated with microstructural changes.
Neural activity has been suggested to initially trigger ATP production by glycolysis, rather than oxidative phosphorylation, for three reasons: glycolytic enzymes are associated with ion pumps; ...neurons may increase their energy supply by activating glycolysis in astrocytes to generate lactate; and activity increases glucose uptake more than O₂ uptake. In rat hippocampal slices, neuronal activity rapidly decreased the levels of extracellular O₂ and intracellular NADH (reduced nicotinamide adenine dinucleotide), even with lactate dehydrogenase blocked to prevent lactate generation, or with only 20% superfused O₂ to mimic physiological O₂ levels. Pharmacological analysis revealed an energy budget in which 11% of O₂ use was on presynaptic action potentials, 17% was on presynaptic Ca²⁺ entry and transmitter release, 46% was on postsynaptic glutamate receptors, and 26% was on postsynaptic action potentials, in approximate accord with theoretical brain energy budgets. Thus, the major mechanisms mediating brain information processing are all initially powered by oxidative phosphorylation, and an astrocyte-neuron lactate shuttle is not needed for this to occur.
•The human brain connectivity literature has been dominated by cortical research.•Subcortical structures are challenging due to lower signal-to-noise ratios.•This review considers the amygdala, ...brainstem, cerebellum and spinal cord.•Anatomical and functional connectivity studies of these structures are reviewed.•Recommendations are given for conducting connectivity analyses beyond the cortex.
Mapping the structural and functional connectivity of the central nervous system has become a key area within neuroimaging research. While detailed network structures across the entire brain have been probed using animal models, non-invasive neuroimaging in humans has thus far been dominated by cortical investigations. Beyond the cortex, subcortical nuclei have traditionally been less accessible due to their smaller size and greater distance from radio frequency coils. However, major neuroimaging developments now provide improved signal and the resolution required to study these structures. Here, we present an overview of the connectivity between the amygdala, brainstem, cerebellum, spinal cord and the rest of the brain. While limitations to their imaging and analyses remain, we also provide some recommendations and considerations for mapping brain connectivity beyond the cortex.
From a gym workout, to deciding whether to persevere at work, many activities require us to persist in deciding that rewards are 'worth the effort' even as we become fatigued. However, studies ...examining effort-based decisions typically assume that the willingness to work is static. Here, we use computational modelling on two effort-based tasks, one behavioural and one during fMRI. We show that two hidden states of fatigue fluctuate on a moment-to-moment basis on different timescales but both reduce the willingness to exert effort for reward. The value of one state increases after effort but is 'recoverable' by rests, whereas a second 'unrecoverable' state gradually increases with work. The BOLD response in separate medial and lateral frontal sub-regions covaried with these states when making effort-based decisions, while a distinct fronto-striatal system integrated fatigue with value. These results provide a computational framework for understanding the brain mechanisms of persistence and momentary fatigue.
Adaptive success in social animals depends on an ability to infer the likely actions of others. Little is known about the neural computations that underlie this capacity. Here, we show that the brain ...models the values and choices of others even when these values are currently irrelevant. These modeled choices use the same computations that underlie our own choices, but are resolved in a distinct neighboring medial prefrontal brain region. Crucially, however, when subjects choose on behalf of a partner instead of themselves, these regions exchange their functional roles. Hence, regions that represented values of the subject’s executed choices now represent the values of choices executed on behalf of the partner, and those that previously modeled the partner now model the subject. These data tie together neural computations underlying self-referential and social inference, and in so doing establish a new functional axis characterizing the medial wall of prefrontal cortex.
► Valuation and choice for self and other exhibit parallel computations in PFC ► vmPFC computes choices that will be executed, whether for self or other ► Rostral dmPFC computes choices that are modeled, whether for self or other ► A similar gradient is present in temporoparietal cortex
Nicolle et al. show that valuation and choice for self and other exhibit parallel computations, where gradients exist within both medial prefrontal and temporoparietal cortices. Ventral regions compute choices that will be executed, while dorsal regions compute choices that are merely modeled.
To navigate social environments, people must simultaneously hold representations about their own and others’ abilities. During self-other mergence, people estimate others’ abilities not only on the ...basis of the others’ past performance, but the estimates are also influenced by their own performance. For example, if we perform well, we overestimate the abilities of those with whom we are co-operating and underestimate competitors. Self-other mergence is associated with specific activity patterns in the dorsomedial prefrontal cortex (dmPFC). Using a combination of non-invasive brain stimulation, functional magnetic resonance imaging, and computational modeling, we show that dmPFC neurostimulation silences these neural signatures of self-other mergence in relation to estimation of others’ abilities. In consequence, self-other mergence behavior increases, and our assessments of our own performance are projected increasingly onto other people. This suggests an inherent tendency to form interdependent social representations and a causal role of the dmPFC in separating self and other representations.
•During self-other mergence (SOM), people confuse one’s own with another’s performance•Brain stimulation over dorsomedial prefrontal cortex (dmPFC) alters neural SOM•Brain stimulation over dmPFC simultaneously alters behavioral SOM•This suggests a causal role of dmPFC in separating self and other representations
Wittmann et al. find that, after disrupting activity in the dorsomedial prefrontal cortex, humans merge performance estimates concerning other people with performance estimates about themselves. This suggests that representations of self and others are inherently interlinked and that intact dmPFC activity is needed for separating the two.
PDF
