Fabian Grabenhorst’s research while affiliated with University of Oxford and other places

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Publications (70)


Whole-brain analysis results related to parametric variables during choice phase (cluster P-values corrected for family-wise error across the whole brain, P < 0.05; maps thresholded at P < 0.001, extent threshold ≥10 voxels). * * Uncorrected at P < 0.005
Neural activity in human ventromedial prefrontal cortex reflecting the intention to save reward
  • Article
  • Full-text available

January 2020

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63 Reads

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5 Citations

Social Cognitive and Affective Neuroscience

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Fabian Grabenhorst

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Wolfram Schultz

Saving behavior usually require individuals to perform several consecutive choices before collecting the final reward. The overt behavior is preceded by an intention to perform an appropriate choice sequence. We studied saving sequences for which each participant rated the intention numerically as willingness-to-save. Each sequence resulted in a specific reward amount and thus had a particular value for the participant, which we assessed with a Becker-DeGroot-Marschak (BDM) auction-like mechanism. Using functional MRI, we found that blood oxygen level dependent (BOLD) signals in human ventromedial prefrontal cortex (vmPFC) correlated with the participant's stated intention before each choice sequence. An adjacent vmPFC region showed graded activation that reflected the value of the sequence. These results demonstrate an involvement of vmPFC in intentional processes preceding sequential economic choices.

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How we choose multi-component rewards

November 2019

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22 Reads

Realistic, everyday rewards contain multiple components. An apple has taste and size. However, we choose in single dimensions, simply preferring some apples to others. How can such single-dimensional relationships refer to multi-dimensional choice options? Here, we investigated stochastic choices of two-component milkshakes. The revealed preferences were intuitively graphed as indifference curves that indicated how much of one component was traded-in for obtaining one unit of the other component without a change in preference, thus defining the orderly integration of multiple components into single-dimensional estimates. Options on higher indifference curves were preferred to those on lower curves. The systematic, non-overlapping curves satisfied leave-one-out tests, followed decoder predictions and correlated with Becker-DeGroot-Marschak auction-like bids. These single-dimensional estimates of multi-component options complied with rigorous concepts of Revealed Preference Theory and encourage formal investigations of normal, irrational and pathological decisions and their neural signals.


Figure 1. Risk, choice task and basic behavior. (A) Relationship between risk measured as reward variance and reward probability. (B) Choice task. The animal made a saccade-choice between two visual stimuli (fractals, 'objects') associated with specific base reward probabilities. Object reward probabilities varied predictably trialby-trial according to a typical schedule for eliciting matching behavior and unpredictably block-wise due to baseprobability changes. Probabilities were uncued, requiring animals to derive reward risk internally from the variance of recently experienced rewards. Left-right object positions varied pseudorandomly. (C) Matching behavior shown in log ratios of rewards and choices. Relationship between log-transformed choice and reward ratio averaged across sessions and animals (N = 16,346 trials; linear regression; equally populated bins of reward ratios; standard errors of the mean (s.e.m.) were smaller than symbols). (D) Cumulative object choices in an example session. The choice ratio in each trial block (given by the slope of the dark blue line) matched the corresponding reward ratio (light blue). (E) Adaptation to block-wise reward-probability changes. Matching coefficient (correlation between choice and reward ratio) calculated using seven-trial sliding window around base probability changes (data across sessions, asterisks indicate significant correlation, p<0.05). DOI: https://doi.org/10.7554/eLife.44838.002 The following source data is available for figure 1:
Comparison of different models fitted to the animals' choices. Best fitting model indicated in bold.
Primate prefrontal neurons signal economic risk derived from the statistics of recent reward experience

July 2019

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123 Reads

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14 Citations

eLife

Risk derives from the variation of rewards and governs economic decisions, yet how the brain calculates risk from the frequency of experienced events, rather than from explicit risk-descriptive cues, remains unclear. Here, we investigated whether neurons in dorsolateral prefrontal cortex process risk derived from reward experience. Monkeys performed in a probabilistic choice task in which the statistical variance of experienced rewards evolved continually. During these choices, prefrontal neurons signaled the reward-variance associated with specific objects ('object risk') or actions ('action risk'). Crucially, risk was not derived from explicit, risk-descriptive cues but calculated internally from the variance of recently experienced rewards. Support-vector-machine decoding demonstrated accurate neuronal risk discrimination. Within trials, neuronal signals transitioned from experienced reward to risk (risk updating) and from risk to upcoming choice (choice computation). Thus, prefrontal neurons encode the statistical variance of recently experienced rewards, complying with formal decision variables of object risk and action risk.


Neural Mechanisms for Accepting and Rejecting Artificial Social Partners in the Uncanny Valley

July 2019

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332 Reads

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64 Citations

The Journal of Neuroscience : The Official Journal of the Society for Neuroscience

Artificial agents are becoming prevalent across human life domains. However, the neural mechanisms underlying human responses to these new, artificial social partners remain unclear. The uncanny valley (UV) hypothesis predicts that humans prefer anthropomorphic agents but reject them if they become too humanlike-the so-called UV reaction. Using fMRI, we investigated neural activity when subjects evaluated artificial agents and made decisions about them. Across two experimental tasks, the ventromedial prefrontal cortex (VMPFC) encoded an explicit representation of subjects' UV reactions. Specifically, VMPFC signaled the subjective likability of artificial agents as a nonlinear function of humanlikeness, with selective low likability for highly humanlike agents. In exploratory across-subject analyses, these effects explained individual differences in psychophysical evaluations and preference choices. Functionally connected areas encoded critical inputs for these signals: the temporoparietal junction encoded a linear humanlikeness continuum, whereas nonlinear representations of humanlikeness in dorsomedial prefrontal cortex (DMPFC) and fusiform gyrus emphasized a human-nonhuman distinction. Following principles of multisensory integration, multiplicative combination of these signals reconstructed VMPFC's valuation function. During decision making, separate signals in VMPFC and DMPFC encoded subjects' decision variable for choices involving humans or artificial agents, respectively. A distinct amygdala signal predicted rejection of artificial agents. Our data suggest that human reactions toward artificial agents are governed by a neural mechanism that generates a selective, nonlinear valuation in response to a specific feature combination (humanlikeness in nonhuman agents). Thus, a basic principle known from sensory coding-neural feature selectivity from linear-nonlinear transformation-may also underlie human responses to artificial social partners.SIGNIFICANCE STATEMENT Would you trust a robot to make decisions for you? Autonomous artificial agents are increasingly entering our lives, but how the human brain responds to these new artificial social partners remains unclear. The uncanny valley (UV) hypothesis-an influential psychological framework-captures the observation that human responses to artificial agents are nonlinear: we like increasingly anthropomorphic artificial agents, but feel uncomfortable if they become too humanlike. Here we investigated neural activity when humans evaluated artificial agents and made personal decisions about them. Our findings suggest a novel neurobiological conceptualization of human responses toward artificial agents: the UV reaction-a selective dislike of highly humanlike agents-is based on nonlinear value-coding in ventromedial prefrontal cortex, a key component of the brain's reward system.


Primate Amygdala Neurons Simulate Decision Processes of Social Partners

April 2019

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592 Reads

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91 Citations

Cell

By observing their social partners, primates learn about reward values of objects. Here, we show that monkeys’ amygdala neurons derive object values from observation and use these values to simulate a partner monkey’s decision process. While monkeys alternated making reward-based choices, amygdala neurons encoded object-specific values learned from observation. Dynamic activities converted these values to representations of the recorded monkey’s own choices. Surprisingly, the same activity patterns unfolded spontaneously before partner’s choices in separate neurons, as if these neurons simulated the partner’s decision-making. These ‘‘simulation neurons’’ encoded signatures of mutual-inhibitory decision computation, including value comparisons and value-to-choice conversions, resulting in accurate predictions of partner’s choices. Population decoding identified differential contributions of amygdala subnuclei. Biophysical modeling of amygdala circuits showed that simulation neurons emerge naturally from convergence between object-value neurons and self-other neurons. By simulating decision computations during observation, these neurons could allow primates to reconstruct their social partners’ mental states.


Author Correction: A dynamic code for economic object valuation in prefrontal cortex neurons

November 2017

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53 Reads

This corrects the article DOI: 10.1038/ncomms12554.



Citations (49)


... In humans and other primates, OFC activity does reflect an identity-based value signal in orthonasally presented odours 46-48 as well as nutrient-guided valuation of visual food stimuli 49,50 . In addition to these anticipatory cues, the human and primate OFC is also sensitive to consummatory reward features such as taste 16,35 , retronasal odour 35,51 and oral texture 52,53 . Given the established role of OFC neurons in encoding the identity and value of offered and chosen oral food stimuli 17 , as well as our finding of crossmodal decoding in the OFC, our results are in line with the idea that the OFC evaluates an integrated flavour signal from the insula. ...

Reference:

Tastes and retronasal odours evoke a shared flavour-specific neural code in the human insula
A Neural Mechanism in the Human Orbitofrontal Cortex for Preferring High-Fat Foods Based on Oral Texture

The Journal of Neuroscience : The Official Journal of the Society for Neuroscience

... Success and failure in these processes have been linked to differential life outcomes and psychiatric conditions. Here we review evidence from single-neuron recordings and neuroimaging studies that implicate the amygdala-a brain structure long associated with cue-reactivity and emotion-in decision-making and the planned pursuit of future rewards (Grabenhorst et al., 2012(Grabenhorst et al., , 2023Hernadi et al., 2015;Zangemeister et al., 2016). The main findings are that, in behavioral tasks in which future rewards can be pursued through planning and stepwise decision-making, amygdala neurons prospectively encode the value of anticipated rewards and related behavioral plans. ...

A view-based decision mechanism for rewards in the primate amygdala
  • Citing Article
  • September 2023

Neuron

... Cross-species research provides invaluable insights, overcoming the conceptual and methodological limitations inherent to human-only or animal-only studies (Polley & Schiller 2022). Recent comparative analyses have begun to unravel the complex neural mechanisms of reward and punishment processing across different species (Bromberg-Martin et al. 2024, Rudebeck & Izquierdo 2022, Wallis 2012, Woo et al. 2023. ...

Mechanisms of adjustments to different types of uncertainty in the reward environment across mice and monkeys

Cognitive Affective & Behavioral Neuroscience

... Parametric variation of non-food reinforcer options could be used to further fractionate rats' preferences and provide more detailed insights into how rats derive utility from engaging with different types of objects. More generally, the free-choice foraging behavioral framework used here could be extended to investigate a wider range of both nutritive (63,64) and non-nutritive (65-68) rewards. ...

Nutrient-Sensitive Reinforcement Learning in Monkeys

The Journal of Neuroscience : The Official Journal of the Society for Neuroscience

... Some studies have examined the specific influences of energy, nutrients, and sensory properties on food selection and the control of feeding in RM. As in humans, high fat and/or carbohydrate contents in test foods are reported to be highly palatable and divert RM from nutritional reference values in a manner suggesting that they assigned value to specific nutrients rather than energy intake per se (79). Consistent with Bremer et al.'s (74) results above, RM regulate energy intake through compensating for gastric preloads of macronutrients by decreasing intake at subsequent feeding periods. ...

Preferences for nutrients and sensory food qualities identify biological sources of economic values in monkeys

Proceedings of the National Academy of Sciences

... The amygdala, a cell complex located in the anterior-medial temporal lobe ( Figure 1A), has long been associated with mediating emotional reactions to sensory cues (Rolls, 2000;Baxter and Murray, 2002;Cardinal et al., 2002;Maren and Quirk, 2004;Balleine and Killcross, 2006;Murray, 2007;Ghods-Sharifi et al., 2009;Morrison and Salzman, 2010;Johansen et al., 2011;Janak and Tye, 2015;Gothard, 2020;Pujara et al., 2022). However, recent findings also implicate primate amygdala neurons in more complex cognitive functions, including the pursuit of future rewards through economic, value-based decision-making and planning (Grabenhorst et al., 2012;Hernadi et al., 2015;Grabenhorst et al., 2016;Grabenhorst et al., 2019;Grabenhorst and Schultz, 2021;Grabenhorst et al., 2023). ...

Functions of primate amygdala neurons in economic decisions and social decision simulation
  • Citing Article
  • April 2021

Behavioural Brain Research

... With these properties, the IA provides for a stringent test framework for investigating brain mechanisms of economic choice. So far, human fMRI studies demonstrate subjective value coding in reward-related brain regions, including the ventral striatum, midbrain, amygdala, and orbitofrontal and ventromedial prefrontal cortex (Gelskov et al., 2015;Hsu et al., 2009;Seak et al., 2021;Wu et al., 2011). Neurophysiological studies in monkeys demonstrate the coding of subjective value in midbrain dopamine neurons and orbitofrontal cortex (Kobayashi & Schultz, 2008;Lak et al., 2014;Padoa-Schioppa & Assad, 2006;Stauffer et al., 2014;Tremblay & Schultz, 1999) and formal utility coding in dopamine neurons . ...

Single-Dimensional Human Brain Signals for Two-Dimensional Economic Choice Options

The Journal of Neuroscience : The Official Journal of the Society for Neuroscience

... Each person has a particular identity that corresponds to their behavior and serves as a paradigm. Identity utility refers to the change in utility that results from the adaptation of individual behavior to identity norms, and utility maximization is a general and fundamental process that determines the subject's survival (Ferrari-Toniolo et al., 2021). In light of this, we proposed to measure identity salience from the perspective of utility, suggesting that the more utility a role brings to an individual, the higher its salience. ...

Nonhuman Primates Satisfy Utility Maximization in Compliance with the Continuity Axiom of Expected Utility Theory

The Journal of Neuroscience : The Official Journal of the Society for Neuroscience

... First, it is assumed that this system learns associations through dopamine mediated reinforcement processes (Ashby & Valentin, 2017). Second, it is assumed that dopamine pathways are relevant for reward processing because they code for unexpected errors (Pastor-Bernier et al., 2020;Schultz, 1999). Because the ALF model updates its coefficients when an error is made, Basal Ganglia circuitry seems like a reasonable biological structure to implement processes like those described in the current work. ...

Experimentally Revealed Stochastic Preferences for Multicomponent Choice Options

Journal of Experimental Psychology: Animal Learning and Cognition

... Our previous work established ICs in rhesus monkeys that represent subjective reward values in an orderly manner and fulfill necessary requirements for rationality, including completeness (preference for one or the other option, or indifference), transitivity, and independence of option set size (Pastor-Bernier et al., 2017). Similar ICs were empirically estimated in humans (Pastor-Bernier et al., 2020). The ICs represent the relative subjective values of the two bundle rewards; thus, important for the present study, IC changes would indicate changes in relative reward value. ...

Experimentally Revealed Stochastic Preferences for Multi-Component Choice Options
  • Citing Article
  • January 2020

SSRN Electronic Journal