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Battaglia Mayer, A.

Publications and source records attributed to Battaglia Mayer, A..

5 recordsLinked to original sources

JOINT ACTION AWARENESS IN MACAQUES DURING A MULTIPLAYER VIDEO-GAME CONTEXT

In behavioral neuroscience, research in nonhuman primates often relies on video game like paradigms, including studies of social interaction and joint action. In social studies, establishing whether animals monitor their partner and are aware of their reciprocal interactions in these abstract laboratory settings is essential for interpreting the processes underlying cooperative performance. Here, we examined spontaneous head orienting behavior in two macaques performing a cooperative visuomotor task under highly controlled conditions. The animals sat side by side with their heads unrestrained and used isometric joysticks to control their respective cursors displayed on a shared screen. Depending on trial instructions, they performed either individual actions (SOLO action, SA) or joint actions (JA) to obtain a reward. We quantified spontaneous head rotations toward the partner as an ethologically relevant behavioral indicator of social monitoring. Partner directed head turns occurred more frequently during JA than during SA trials. Crucially, their rate increased with the number of errors made by the partner during JA trials. Together, these findings indicate that macaques monitor their partner during abstract, computer-mediated cooperative interactions and that this monitoring is driven by the performance of the partner. Such spontaneous, context specific orienting toward the partner supports the interpretation that macaques are aware of their dyadic engagement, even in video game like settings. Our results therefore highlight the suitability of controlled visuomotor paradigms for investigating the cognitive-motor processes underlying joint action in nonhuman primates.

neuroscience↗

COSTS AND BENEFITS OF ACTING TOGETHER: A NON-HUMAN PRIMATE MODEL OF COOPERATIVE DECISION-MAKING

Cooperation is a crucial aspect of social behavior, allowing individuals to achieve goals unattainable alone. However, collective actions require costly inter-individual coordination, making continuous cost-benefit evaluation essential before engaging in cooperation. Non-human primate models can help uncover the evolutionary foundations of human cooperation and its underlying neural mechanisms. To this aim, we developed a novel paradigm to analyze the dyadic behavior of two macaques, who took turns in choosing between individual and cooperative actions to obtain variable rewards. Each monkey used a joystick to guide a cursor toward one of two targets, each indicating both the reward magnitude and the action type (i.e. solo action or joint action) required to obtain their payoff. We first observed a linear improvement in dyadic performance with the expected reward magnitude. Although macaques tended to prefer individual actions, they selected to act jointly under favorable payoff conditions, indicating that voluntary cooperation in macaques can emerge as a reward-driven process. Logistic models of their choices revealed the subjective cost monkeys assigned to cooperation, which was consistent across subjects. Nonetheless, the gain rate across different sessions increased over time, suggesting that macaques possess the cognitive ability to optimize their dyadic strategies, by estimating not only the coordination costs but also the benefits of cooperation. We observed a progressive reduction in the subjective cost assigned to joint action, which was not directly dependent on performance improvements. Our findings suggest that non-human primates can weigh the costs and benefits of cooperation, highlighting their ability to dynamically adjust social strategies based on reward contingencies. HIGHLIGHTS- Expected reward magnitude enhances cooperative performance in macaques - Monkeys evaluate the cost-benefit trade-off of cooperative actions in social contexts - In macaques, the subjective cost of cooperation decreases over time, promoting a gradual shift toward a pro-social strategy that maximizes outcomes - Cooperative behavior in macaques can emerge as a reward-driven, cost-benefit decision process - Macaques may exhibit metacognitive dynamics, using internal evaluations of expected outcomes to guide collective behavior

neuroscience↗

How Acting Jointly Differs from Acting Side-by-Side: A Dual EEG Study

The distinction between acting jointly and acting side by side permeates our daily lives and is crucial for understanding the evolution and development of human sociality. While acting in parallel involves agents pursuing individual goals, acting jointly requires them to share a collective goal. Here, we used a dual electroencephalography (EEG) approach to explore the neural dynamics underlying joint and parallel action preparation. We recorded event-related potentials (ERPs) from 20 dyads while they had to transport an object in a video game, either jointly or in parallel, or individually. Both conditions were carefully matched for coordination demands and performance complexity, as confirmed by equal success rates. Our results revealed a distinctive pattern swap in ERPs during action preparation. In the early preparation phase, ERPs showed significantly higher amplitude during joint action than parallel action. This pattern reversed in the late preparation phase, with significantly reduced ERP amplitude in the joint compared to parallel action. Notably, the decrease in late ERPs correlated with higher reaction time (RT) variability in partners but not with participants own RT variability. The dynamic swap in neural activity suggests that different cognitive processes operate at distinct stages of action preparation. While initially sharing a collective goal may impose cognitive costs (reflected in higher early ERPs), this is offset by facilitated late action preparation, likely due to enhanced predictability of partners actions. Significance StatementOur study reveals distinct neural signatures differentiating joint from side-by-side actions. Through dual EEG recordings of twenty dyads performing complexity-matched tasks, we identified a distinctive "swap" in event-related potentials during action preparation. Joint actions initially showed higher early-phase amplitudes but significantly reduced late-phase amplitudes compared to parallel actions. Notably, this late-phase reduction correlated specifically with the variability of partners behavior. This suggests that sharing collective goals initially requires cognitive resources but facilitates action preparation through enhanced predictability of partners. These findings provide a neural framework for understanding the distinction between acting jointly and acting in parallel --a distinction that pervades our daily experiences and is crucial for understanding the development and evolution of human sociality.

neuroscience↗

A cortical mechanism linking saliency detection and motor reactivity in rhesus monkeys

Sudden and surprising sensory events trigger neural processes that swiftly adjust behavior. To study the phylogenesis and the mechanism of this phenomenon, we trained two rhesus monkeys to keep a cursor inside a visual target by exerting force on an isometric joystick. We examined the effect of surprising auditory stimuli on exerted force, scalp electroencephalographic (EEG) activity, and local field potentials (LFP) recorded from the dorso-lateral prefrontal cortex. Auditory stimuli elicited (1) a biphasic modulation of isometric force: a transient decrease followed by a corrective tonic increase, and (2) EEG and LFP deflections dominated by two large negative-positive waves (N70 and P130). The EEG potential was maximal at the scalp vertex, in all respects similar to the human vertex potential. Electrocortical potentials and force were tightly coupled: the P130 amplitude predicted the magnitude of the corrective force increase, particularly in the EEG electrodes contralateral to the limb exerting force, and in the LFP recorded from deep rather than superficial cortical layers, suggesting a direct effect of the vertex potential on the motor output determining the behavior. These results disclose a phylogenetically-preserved cortico-motor mechanism supporting adaptive behavior in response to salient sensory events.

neuroscience↗

THE COMPLEX HODOLOGICAL ARCHITECTURE OF THE MACAQUE DORSAL INTRAPARIETAL AREAS AS EMERGING FROM NEURAL TRACERS AND DW-MRI TRACTOGRAPHY

In macaque monkeys, dorsal intraparietal areas are involved in several daily visuo-motor actions. However, their border and sources of cortical afferents remain loosely defined. Through a retrograde tracer and MRI diffusion-based tractography study here we show a complex organization of the dorsal bank of the IPS, which can be subdivided into a rostral area PEip, projecting to the spinal cord, and a caudal area MIP lacking such projections. Both areas include a rostral and a caudal sector, emerging from their ipsilateral, gradient-like connectivity profiles. As tractography estimations, we used the cross-sectional volume of the white matter bundles connecting each area with other parietal and frontal regions, after selecting ROIs corresponding to the injection sites of retrograde tracers. A quantitative analysis between the proportions of cells projecting to all sectors of PEip and MIP along the continuum of the dorsal bank of the IPS and tractography revealed a significant correlation between the two data sets for most connections. Moreover, tractography revealed "false positive" but plausible streamlines awaiting histological validation.

neuroscience↗