Four core properties of the human brain valuation system demonstrated in intracranial signals

Lopez-Persem, Alizée; Bastin, Julien; Petton, Mathilde; Abitbol, Raphaëlle; Lehongre, Katia; Adam, Claude; Navarro, Vincent; Rheims, Sylvain; Kahane, Philippe; Domenech, Philippe; Pessiglione, Mathias

doi:10.1038/s41593-020-0615-9

Cited by 90 publications

(150 citation statements)

References 52 publications

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“…Besides, HERs modulated value encoding in a multiplicative manner. Our results thus differ from a previously reported vmPFC baseline-shift additive effect in pleasantness ratings (Abitbol et al, 2015;Lopez-Persem et al, 2020). Altogether, our results indicate that part of the unspecified 'neural noise' driving fluctuations in choice consistency (Padoa-Schioppa, 2013;Kurtz-David et al, 2019;Webb et al, 2019) comes from the interaction between interoceptive self-related processes, indexed by neural monitoring of cardiac signals, and the neural encoding of subjective value.…”

Section: Discussioncontrasting

confidence: 99%

Responses to heartbeats in ventromedial prefrontal cortex contribute to subjective preference-based decisions

Azzalini

Buot

Palminteri

et al. 2019

Preprint

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Forrest Gump or Matrix? Choosing which movie you prefer is a subjective decision that entails self-reflection. While the neural underpinnings of valuation and choice have been extensively investigated, the contribution of self-related processes to subjective decisions has been largely overlooked. Self-related processes have been linked to a basic interoceptive biological mechanism, the neural monitoring of heartbeats, in particular in ventromedial prefrontal cortex (vmPFC), a region also involved in value encoding. We thus hypothesized a functional coupling between interoceptive self-related processes and the precision of value encoding in vmPFC. Human participants were presented with pairs of movie titles. They indicated either which movie they preferred, or performed a control objective visual discrimination that did not require self-reflection. Using magnetoencephalography, we measured heartbeat-evoked responses (HERs) before option presentation, and confirmed that HERs in vmPFC were larger when preparing to the subjective, self-related task. We retrieved the expected cortical value network during choice with time-resolved statistical modeling, and show that HERs before option presentation interacted in a multiplicative manner with value encoding during choice in vmPFC. The interaction was absent in the objective discrimination task, and could not be trivially explained neither by changes in cardiac activity nor by arousal fluctuations. The neural interaction between HERs and value encoding predicted preference-based choice consistency over time, accounting for both inter-individual differences and trial-to-trial fluctuations within individuals. Our results thus reveal a functional coupling in vmPFC between self-related interoceptive processes and subjective value encoding, which stabilizes the behavioral expression of long-term preferences.Significance statementDeciding whether you prefer Forrest Gump or Matrix is based on subjective values, which only you, the decision-maker, can estimate and compare, by asking yourself. Yet, how self-related processes influence subjective valuation is not known. We show that in ventromedial prefrontal cortex, an interoceptive self-related process, the neural response to heartbeats, influences the cortical representation of subjective value. The neural interaction between interoceptive self-related process and value encoding predicts choice consistency, i.e. whether you consistently prefer Forrest Gump over Matrix over time, thus contributing to the stable expression of long-lasting preferences that define, at least in part, our identity.

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Section: Discussioncontrasting

confidence: 99%

Responses to heartbeats in ventromedial prefrontal cortex contribute to subjective preference-based decisions

Azzalini

Buot

Palminteri

et al. 2019

Preprint

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“…Yet when the different frequency bands were put in competition for predicting PE across trials, low-frequency activity proved to be redundant, with respect to the information already contained in BGA. This result is in line with our analysis of subjective valuation for decision making (Lopez-Persem et al, 2020): all the information available in neural activity could be found in BGA, even if activity in lower-frequency bands also showed significant value signals.…”

Section: Specification Of Pe Signalssupporting

confidence: 90%

“…Indeed, manipulation of dopaminergic transmission was found to interfere with reward learning, specifically (Bodi et al, 2009;Frank, 2004;Rutledge et al, 2009), an effect that was captured by reward sensitivity in a computational model of learning in this task (Pessiglione et al 2006).The observation of reward PE signals in the lOFC was less expected, because it is generally not reported in meta-analyses of human fMRI studies and because several electrophysiology studies in animals suggested that, even if orbitofrontal cortex neurons respond to reward outcomes, they might not encode prediction errors (Roesch et al, 2010;Schultz, 2000). However, the similarity between lOFC and vmPFC reward PE signals is consistent with previous iEEG studies showing similar representation of subjective value and reward outcome in the two regions BGA (Lopez-Persem et al, 2020;Saez et al, 2018). Yet the lOFC and vmPFC reward PE signals may serve different functions, as was suggested by lesion studies in both human and non-human primates showing that the lOFC (but not the vmPFC) is critical for solving the credit assignment problem (Noonan et al, 2010(Noonan et al, , 2017.…”

Section: Dissociation Between Reward and Punishment Pesupporting

confidence: 71%

Opponent intracerebral signals for reward and punishment prediction errors in humans

Gueguen

Billeke

Lachaux

et al. 2020

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Whether maximizing rewards and minimizing punishments rely on distinct brain systems remains debated, inconsistent results coming from human neuroimaging and animal electrophysiology studies. Bridging the gap across species and techniques, we recorded intracerebral activity from twenty patients with epilepsy while they performed an instrumental learning task. We found that both reward and punishment prediction errors (PE), estimated from computational modeling of choice behavior, correlated positively with broadband gamma activity (BGA) in several brain regions. In all cases, BGA increased with both outcome (reward or punishment versus nothing) and surprise (how unexpected the outcome is). However, some regions (such as the ventromedial prefrontal and lateral orbitofrontal cortex) were more sensitive to reward PE, whereas others (such as the anterior insula and dorsolateral prefrontal cortex) were more sensitive to punishment PE. Thus, opponent systems in the human brain might mediate the repetition of rewarded choices and the avoidance of punished choices.

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“…As such, our findings suggest that the contribution of OFC to decision making may be limited to situations that require model-based planning, and that choices based on direct experience may rely on value computations in other brain areas, such as the amygdala or striatum (Paton et al, 2006;Cox and Witten, 2019). This proposal is seemingly at odds with a large number of studies across different species that has shown neural correlates of both inferred and directly experienced value in OFC (Hare et al, 2009;Schoenbaum et al, 2009;Barron et al, 2013;Stalnaker et al, 2014;Howard et al, 2015;Padoa-Schioppa and Conen, 2017;Suzuki et al, 2017;Klein-Flugge et al, 2019;Lopez-Persem et al, 2020;Wang et al, 2020). Why would OFC represent value signals if they are not required for behavior?…”

Section: Discussionmentioning

confidence: 72%

Targeted stimulation of an orbitofrontal network disrupts decisions based on inferred, not experienced outcomes

Wang

Howard

Voss

et al. 2020

Preprint

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ABSTRACTWhen direct experience is unavailable, animals and humans can imagine or infer the future to guide decisions. Behavior based on direct experience versus inference may recruit distinct but overlapping brain circuits. In rodents, the orbitofrontal cortex (OFC) contains neural signatures of inferred outcomes, and OFC is necessary for behavior that requires inference but not for responding driven by direct experience. In humans, OFC activity is also correlated with inferred outcomes, but it is unclear whether OFC activity is required for inference-based behavior. To test this, we used non-invasive network-based continuous theta burst stimulation (cTBS) to target lateral OFC networks in the context of a sensory preconditioning task that was designed to isolate inference-based behavior from responding that can be based on direct experience alone. We show that relative to sham, cTBS targeting this network impairs reward-related behavior in conditions in which outcome expectations have to be mentally inferred. In contrast, OFC-targeted stimulation does not impair behavior that can be based on previously experienced stimulus-outcome associations. These findings suggest that activity in the targeted OFC network supports decision making when outcomes have to be mentally simulated, providing converging cross-species evidence for a critical role of OFC in model-based but not model-free control of behavior.

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Four core properties of the human brain valuation system demonstrated in intracranial signals

Cited by 90 publications

References 52 publications

Responses to heartbeats in ventromedial prefrontal cortex contribute to subjective preference-based decisions

Responses to heartbeats in ventromedial prefrontal cortex contribute to subjective preference-based decisions

Opponent intracerebral signals for reward and punishment prediction errors in humans

Targeted stimulation of an orbitofrontal network disrupts decisions based on inferred, not experienced outcomes

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