Biology subjects

Ferrari-Toniolo, S.

Publications and source records attributed to Ferrari-Toniolo, S..

10 recordsLinked to original sources

bioRxiv2025

Value coding by primate amygdala neurons complies with economic choice theory

Primate amygdala neurons are implicated in coding the value of choice options for decision-making. However, it remains unclear whether amygdala value signals comply with the notion that decision makers maximize the value of rewards, as formalized by key axioms of economic theory. In particular, the continuity axiom of Expected Utility Theory (EUT) postulates that reward maximization is reflected by a trade-off between reward probability and magnitude. Our experiment tested this trade-off in two male macaque monkeys who subjectively ranked three gambles in choices, thus revealing their subjective value. Axiom compliance was defined by choice indifference between the intermediate gamble and a probabilistic combination of the other two gambles. We found that the animals choices between safe and gamble options reflected the integration of probability and magnitude into scalar values consistent with the continuity axiom. In a non-choice task, responses of individual amygdala neurons to separate probability and magnitude cues reflected the monkeys individual preferences: neuronal responses were lower for non-preferred gambles (relative to safe options), higher for preferred gambles and equal at subjective indifference between safe and gamble options. In a choice task, amygdala neurons integrated probability and magnitude into subjective values that reflected individual preferences. In some neurons, value signals transitioned to signals coding the monkeys economic choices and chosen values. These findings identify amygdala neurons as substrates for encoding behavior-matching subjective values according to the continuity axiom of EUT, and for translating these values into economic choices. SIGNIFICANCE STATEMENTThe amygdala--a brain structure in the temporal lobe--has long been associated with emotional responses. More recently, primate amygdala neurons have been implicated in economic decision-making. Here we show that amygdala neurons respond to visual cues indicating reward probability and magnitude in a manner that reflects the integration of these variables into subjective values. Importantly, these value signals complied with the notion that decision makers maximize the value of rewards, as formalized by key axioms of economic theory. Beyond valuation, some neurons processed subjective values into signals predictive of economic choices. Dysfunctional processing of values and choices by the amygdala could play a role in psychiatric and behavioral disorders affecting mental health, in which the amygdala is implicated.

neuroscience↗

bioRxiv2025

Coding of the basic components of subjective value in primate dopamine neurons: subjectively weighted reward amount and probability

Behavioral choices of uncertain rewards suggest that agents construct subjective reward value by combining the basic value components of utility and weighted probability. Despite the general acceptance of this evaluation mechanism for explaining economic choice, knowledge about its neuronal implementation is fractionated and remains essentially unknown. We investigated in monkeys whether reward signals in dopamine neurons might represent subjective reward value based on these two fundamental value components. Despite some heterogeneity across individual neurons, the dopamine population signal reliably represented the axiomatically defined integration of utility and weighted probability into subjective value in a way that closely matched the animal-specific choice behavior. In particular, we identified a crucial contribution of subjectively weighted probability to the dopamine signal of subjective reward value. These data demonstrate a neuronal implementation of subjective value constructed from the two most basic subjective reward components. Preprint ServerAn earlier version of this manuscript has been uploaded to bioRxiv in February 2025 (CC-BY).

neuroscience↗

bioRxiv2023

Systematic comparison of risky choices in humans and monkeys

The past decades have seen tremendous progress in fundamental studies on economic choice in humans. However, elucidation of the underlying neuronal processes requires invasive neurophysiological studies that are met with difficulties in humans. Monkeys as evolutionary closest relatives offer a solution. The animals display sophisticated and well-controllable behavior that allows to implement key constructs of proven economic choice theories. However, the similarity of economic choice between the two species has never been systematically investigated. We investigated compliance with the independence axiom (IA) of expected utility theory as one of the most demanding choice tests and compared IA violations between humans and monkeys. Using generalized linear modeling and cumulative prospect theory (CPT), we found that humans and monkeys made comparable risky choices, although their subjective values (utilities) differed. These results suggest similar fundamental choice mechanism across these primate species and encourage to study their underlying neurophysiological mechanisms.

neuroscience↗

bioRxiv2021

Probability weighting explains Independence Axiom violations of Expected Utility Theory in monkeys

Expected Utility Theory (EUT) provides axioms for maximizing utility in risky choice. The Independence Axiom (IA) is its most demanding axiom: preferences between two options should not change when altering both options equally by mixing them with a common gamble. We tested common consequence (CC) and common ratio (CR) violations of the IA over several months in thousands of stochastic choices using a large variety of binary option sets. Three monkeys showed consistently few outright Preference Reversals (8%) but substantial graded Preference Changes (46%) between the initial preferred gamble and the corresponding altered gamble. Linear Discriminant Analysis (LDA) indicated that gamble probabilities predicted most Preference Changes in CC (72%) and CR (88%) tests. The Akaike Information Criterion indicated that probability weighting within Cumulative Prospect Theory (CPT) explained choices better than models using Expected Value (EV) or EUT. Fitting by utility and probability weighting functions of CPT resulted in nonlinear and non-parallel indifference curves (IC) in the Marschak-Machina triangle and suggested IA non-compliance of models using EV or EUT. Indeed, CPT models predicted Preference Changes better than EV and EUT models. Indifference points in out-of-sample tests were closer to CPT-estimated ICs than EV and EUT ICs. Finally, while the few outright Preference Reversals may reflect the long experience of our monkeys, their more graded Preference Changes corresponded to those reported for humans. In benefitting from the wide testing possibilities in monkeys, our stringent axiomatic tests contribute critical information about risky decision-making and serve as basis for investigating neuronal decision mechanisms.

animal behavior and cognition↗

bioRxiv2021

Reliable population utility signal from diverse economic value coding in orbitofrontal neurons

Behavior-related neuronal signals often vary between neurons. Despite the unreliability of individual neurons, brains are able to accurately represent and drive behavior. The notion may also apply to economic ( value-based) choices and the underlying reward signals. Reward value is subjective and can be defined by nonlinear weighting of magnitude (utility) and probability. Using a wide variety of reward magnitude and probability, we assessed subjective reward value at choice indifference between safe and risky rewards as prescribed by the continuity axiom that provides stringent criteria for meaningful choice. We found that individual neurons in the orbitofrontal cortex (OFC) of monkeys carry unreliable and heterogeneous neuronal signals for subjective value that largely fails to match the animals choice. However, the averaged neuronal signals matched well the animals choices, suggesting reliable subjective economic value encoding by the observed population of unreliable neurons. HighlightsO_LIDifferent from widely held views, reliable neuronal information processing may not require reliable processors. C_LIO_LINeurons in monkey orbitofrontal cortex (OFC) process reward magnitude and probability heterogeneously and unreliably. C_LIO_LIDespite unreliable neuronal processing, OFC population activity codes choices reliably. C_LIO_LIReliability systems performance from unreliable elements seems to be a broad feature of neuronal reward coding. C_LI In briefUsing stringent concepts of behavioral choice, Ferrari-Toniolo and Schultz describe unreliable individual reward neurons in monkey orbitofrontal cortex whose activity combines to a reliable population code for economic choice.

neuroscience↗

bioRxiv2021

Evidence Of We-Representation In Monkeys When Acting Together

A hallmark of successful evolution resides in the ability to adapt our actions to those of others, optimizing collective behaviour, to achieve goals otherwise unattainable by individuals acting alone. We have previously shown that macaques constitute a good model to analyse joint behavior, since they are able to coordinate their actions in a dyadic context. In the present work, we investigated whether monkeys could improve their joint-action performance, under special visuomotor conditions. The behavior of 5 monkeys was analyzed in isometric center-out tasks, requiring hand force application in different directions, either individually or together with a partner. Manipulating the presence or absence of a pre-instruction about the future action condition (SOLO or TOGETHER), allowed us to investigate on the existence of a "we-representation" in macaque monkeys. We found that pre-cueing the future action context increased the chances of dyadic success, also thanks to the emergence of an optimal kinematic setting, that ultimately facilitates inter-individual motor coordination. Our results offer empirical evidence in macaques of a "We-representation" during collective behavior, that once is cued in advance has an overall beneficial effect on joint performance.

animal behavior and cognition↗

bioRxiv2021

Comparing utility functions between risky and riskless choice in rhesus monkeys

Decisions can be risky or riskless, depending on the outcomes of the choice. Expected Utility Theory describes risky choices as a utility maximization process: we choose the option with the highest subjective value (utility), which we compute considering both the options value and its associated risk. According to the random utility maximization framework, riskless choices could also be based on a utility measure. Neuronal mechanisms of utility-based choice may thus be common to both risky and riskless choices. This assumption would require the existence of a utility function that accounts for both risky and riskless decisions. Here, we investigated whether the choice behavior of macaque monkeys in riskless and risky decisions could be described by a common underlying utility function. We found that the utility functions elicited in the two choice scenarios were different from each other, even after taking into account the contribution of subjective probability weighting. Our results suggest that distinct utility representations exist for riskless and risky choices, which could reflect distinct neuronal representations of the utility quantities, or distinct brain mechanisms for risky and riskless choices. The different utility functions should be taken into account in neuronal investigations of utility-based choice.

animal behavior and cognition↗

bioRxiv2020

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 cursors 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. HIGHLIGHTSO_LIIn PMd neural dynamics is shared across action execution and mere observation C_LIO_LITask directional features are more accurately discriminated than action types C_LIO_LISpatial aspects are encoded in PMd independently from specific behavioral demands C_LIO_LIPMd dynamics largely reflect higher cognitive-motor processes rather than strictly motor-related functions C_LI

neuroscience↗

bioRxiv2020

Adaptation of utility functions to reward distribution in rhesus monkeys

This study investigated the influence of experienced reward distributions on the shape of utility functions inferred from economic choice. Utility is the hypothetical variable that appears to be maximized by the choice. Despite the generally accepted notion that utility functions are not insensitive to external references, the exact occurrence of such changes remains largely unknown. Here we benefitted from the capacity to perform thorough and extensive experimental tests of one of our evolutionary closest, experimentally viable and intuitively understandable species, the rhesus macaque monkey. Data from thousands of binary choices demonstrated that the animals preferences changed dependent on the statistics of recently experienced rewards and adapted to future expected rewards. The elicited utility functions shifted and extended their shape with several months of changes in the mean and range of reward distributions. However, the adaptations were usually not complete, suggesting that past experiences remained present when anticipating future rewards. Through modelling, we found that reinforcement learning provided a strong basis for explaining these adaptations. Thus, rather than having stable and fixed preferences assumed by normative economic models, rhesus macaques flexibly shaped their preferences to optimize decision-making according to the statistics of the environment.

animal behavior and cognition↗

bioRxiv2020

Compliance with the continuity axiom of Expected Utility Theory supports utility maximization in monkeys

Expected Utility Theory (EUT), the first axiomatic theory of risky choice, describes choices as a utility maximization process: decision makers assign a subjective value (utility) to each choice option and choose the one with the highest utility. The continuity axiom, central to EUT and its modifications, is a necessary and sufficient condition for the definition of numerical utilities. The axiom requires decision makers to be indifferent between a gamble and a specific probabilistic combination of a more preferred and a less preferred gamble. While previous studies demonstrated that monkeys choose according to combinations of objective reward magnitude and probability, a concept-driven experimental approach for assessing the axiomatically defined conditions for maximizing subjective utility by animals is missing. We experimentally tested the continuity axiom for a broad class of gamble types in four male rhesus macaque monkeys, showing that their choice behavior complied with the existence of a numerical utility measure as defined by the economic theory. We used the numerical quantity specified in the continuity axiom to characterize subjective preferences in a magnitude-probability space. This mapping highlighted a trade-off relation between reward magnitudes and probabilities, compatible with the existence of a utility function underlying subjective value computation. These results support the existence of a numerical utility function able to describe choices, allowing for the investigation of the neuronal substrates responsible for coding such rigorously defined quantity. SIGNIFICANCE STATEMENTA common assumption of several economic choice theories is that decisions result from the comparison of subjectively assigned values (utilities). This study demonstrated the compliance of monkey behavior with the continuity axiom of Expected Utility Theory, implying a subjective magnitude-probability trade-off relation which supports the existence of numerical subjective utility directly linked to the theoretical economic framework. We determined a numerical utility measure able to describe choices, which can serve as a correlate for the neuronal activity in the quest for brain structures and mechanisms guiding decisions.

animal behavior and cognition↗