Search bioRxiv⌕ Search

Biology subjects

Dal Monte, O.

Publications and source records attributed to Dal Monte, O..

8 recordsLinked to original sources

Cross-Category Invariant Neurons in the Human Amygdala

Recognizing individuals or objects across different contexts is a hallmark of primate cognition. Beyond recognition, the brain organizes visual stimuli into meaningful categories, supporting efficient perception and adaptive behavior. Previous studies in the human temporal lobe have identified concept cells supporting invariant representations of specific stimuli. However, invariant coding alone cannot account for how categorical knowledge is structured across related visual domains. Here, we analyzed single-neuron recordings from the human amygdala during the presentation of familiar visual stimuli spanning multiple categories. Using a novel data-driven analytic framework that integrates supervised population decoding with single-neuron analyses, we identified a population of cross-category invariant neurons. These neurons preserved exemplar-invariant responses while generalizing across multiple categories linked by shared naturalistic or human/domestic contexts. Our findings demonstrate that the human amygdala supports both invariant and associative forms of categorical representations. By linking stable identity representations across contextually related categories, the amygdala provides a flexible neural substrate for high-level visual organization, supporting efficient perception and adaptive behavior in complex environments. HighlightsO_LIHuman amygdala neurons encode invariant category representations at the single-cell level C_LIO_LICategory representations are organized according to naturalistic and social contexts C_LIO_LICross-category invariant neurons bridge concept-cell and mixed-selectivity coding C_LIO_LICategory encoding relies on opponent patterns of enhancement and suppression across domain C_LI

neuroscience↗

Causal Dynamics of Social Gaze in Primate Prefrontal-Amygdala Networks Revealed by Dynamic Bayesian Modeling

Social gaze is a fundamental channel of primate communication, shaping dynamic interactions and fostering mutual understanding. While prior studies have mapped the behavioral correlates of social gaze across the prefrontal-amygdala circuits, the causal architecture of these interactions remains poorly understood. Here, we introduce a novel algorithm to integrate independently recorded sessions into "super-sessions", validated using ground-truth synthetic data, enabling the reconstruction of simultaneous multi-area recordings aligned to matched gaze sequences. Applying Dynamic Bayesian Network analysis to these super-sessions, we uncover temporally structured, behavior-dependent causal interactions among the amygdala, orbitofrontal cortex, dorsomedial prefrontal cortex (dmPFC), and anterior cingulate cortex. When macaques were the targets of social gaze, the brain-behavior network exhibited positive temporal modulations, with the dmPFC emerging as the dominant source and the amygdala as a primary recipient of influence. When macaques directed their gaze toward their partners, the dmPFC and amygdala retained their respective roles. Prefrontal regions positively modulated one another, while the amygdala acted solely as a downstream target receiving exclusively negatively modulated prefrontal inputs. These findings reveal previously unknown directional interactions in the primate social brain and highlight distinct causal architectures underlying the bidirectional dynamics of social attention.

neuroscience↗

Compositionality of social gaze in the prefrontal-amygdala circuits

Social gaze underpins primate communication, yet the neural principles enabling its flexibility remain unknown. Each social gaze can be deconstructed into three primitives: gaze content, social state, and gaze duration. To reduce dimensionality and facilitate generalization, the brain needs to represent these primitives in an abstract format. Here we show that social gaze is governed by a compositional code built from these primitives in the brain. In male and female macaques (neural recordings in two males) engaged in real-life social gaze interaction, behavior analyses revealed that partner responses were determined by how primitives were combined, rather than by their independent sums, providing evidence for behavioral compositionality. The basolateral amygdala and the anterior cingulate gyrus represented content and state in an abstract format and orthogonally to one another, whereas the dorsomedial prefrontal and orbitofrontal cortices exhibited limited generalization. Linear mixed-selective neurons encoding both content and state in the basolateral amygdala and the anterior cingulate gyrus, but not in the other two areas, facilitated the abstraction underlying generalization. Moreover, distinct channels routed content and state information across prefrontal-amygdala circuits to minimize interference, which was mediated by linear mixed selectivity neurons. These findings identify a neural grammar for social gaze, revealing compositional computations as a principle of flexible social communication.

neuroscience↗

An unbiased method to partition diverse neuronal responses into functional ensembles reveals interpretable population dynamics during innate social behavior

In neuroscience, understanding how single-neuron firing contributes to distributed neural ensembles is crucial. Traditional methods of analysis have been limited to descriptions of whole population activity, or, when analyzing individual neurons, criteria for response categorization varied significantly across experiments. Current methods lack scalability for large datasets, fail to capture temporal changes and rely on parametric assumptions. Theres a need for a robust, scalable, and non-parametric functional clustering approach to capture interpretable dynamics. To address this challenge, we developed a model-based, statistical framework for unsupervised clustering of multiple time series datasets that exhibit nonlinear dynamics into an a-priori-unknown number of parameterized ensembles called Functional Encoding Units (FEUs). FEU outperforms existing techniques in accuracy and benchmark scores. Here, we apply this FEU formalism to single-unit recordings collected during social behaviors in rodents and primates and demonstrate its hypothesis-generating and testing capacities. This novel pipeline serves as an analytic bridge, translating neural ensemble codes across model systems.

neuroscience↗

Closed-loop microstimulations of the orbitofrontal cortex during real-life gaze interaction enhance dynamic social attention

The prefrontal cortex is extensively involved in social exchange. During dyadic gaze interaction, multiple prefrontal areas exhibit neuronal encoding of social gaze events and context-specific mutual eye contact, supported by a widespread neural mechanism of social gaze monitoring. To explore causal manipulation of real-life gaze interaction, we applied weak closed-loop microstimulations that were precisely triggered by specific social gaze events to three prefrontal areas in monkeys. Microstimulations of orbitofrontal cortex (OFC), but not dorsomedial prefrontal or anterior cingulate cortex, enhanced momentary dynamic social attention in the spatial dimension by decreasing distance of ones gaze fixations relative to partner monkeys eyes. In the temporal dimension, microstimulations of OFC reduced the inter-looking interval for attending to another agent and the latency to reciprocate others directed gaze. These findings demonstrate that primate OFC serves as a functionally accessible node in controlling dynamic social attention and suggest its potential for a therapeutic brain interface.

neuroscience↗

Single-cell foundations of live social gaze interaction in the prefrontal cortex and amygdala

Social gaze interaction powerfully shapes interpersonal communication in humans and other primates. However, little is known about the neural underpinnings of these social behavioral exchanges. Here, we studied neural responses associated with naturalistic, face-to-face, social gaze interactions between pairs of macaques. We examined spiking activity in a large number of neurons spanning four different brain regions involved in social behaviors - the amygdala, orbitofrontal cortex, anterior cingulate cortex, and dorsomedial prefrontal cortex. We observed widespread single-cell representations of social gaze interaction functionalities in these brain regions - social discriminability, social gaze monitoring, and mutual eye contact selectivity. Many of these neurons discriminated looking at social versus non-social stimuli with rich temporal heterogeneity, or parametrically tracked the gaze positions of oneself or the conspecific. Furthermore, many neurons displayed selectivity for mutual eye contact as a function of the initiator or follower of mutual gaze events. Crucially, a significant proportion of neurons coded for more than one of these three signatures of social gaze interaction, supporting the recruitment of partially overlapping neuronal ensembles. Our findings emphasize integrated contributions of the amygdala and prefrontal circuits within the social interaction networks in processing real-life social interactions.

neuroscience↗

Increasing central serotonin with 5-HTP disrupts the inhibition of social gaze in non-human primates

To competently navigate the world, individuals must flexibly balance distinct aspects of social gaze, orienting toward others and inhibiting orienting responses, depending on the context. These behaviors are often disrupted in patient populations treated with serotonergic drugs. However, the field lacks a clear understanding of how the serotonergic system mediates social orienting and inhibiting behaviors. Here, we tested how increasing central concentrations of serotonin with the direct precursor 5-Hydroxytryptophan (5-HTP) would modulate the ability of rhesus macaques to use eye movements to flexibly orient to, or inhibit orienting to, faces. Systemic administrations of 5-HTP effectively increased central serotonin levels and impaired flexible orientation and inhibition. Critically, 5-HTP selectively impaired the ability of monkeys to inhibit orienting to face images, whereas it similarly impaired orienting to face and control images. 5-HTP also caused monkeys to perseverate on their gaze responses, making them worse at flexibly switching between orientating and inhibiting behaviors. Furthermore, the effects of 5-HTP on performance correlated with a constriction of the pupil, an increased time to initiate trials, and an increased reaction time, suggesting that the disruptive effects of 5-HTP on social gaze behaviors are likely driven by a downregulation of arousal and motivational states. Taken together, these findings provide causal evidence for a modulatory relationship between 5-HTP and social gaze behaviors in non-human primates and offer translational insights for the role of the serotonergic system in social gaze.

neuroscience↗

Autonomic arousal tracks outcome salience not valence in monkeys making social decisions

The evolutionary and neural underpinnings of human prosociality are still largely unknown. A growing body of evidence suggests that some species find the sight of another individual receiving a reward reinforcing, often called vicarious reinforcement. One hypothesis is that vicarious reward is reinforcing because it is arousing like a primary reward. We evaluated this hypothesis by measuring the autonomic pupil response of eight monkeys across two laboratories in two different versions of a vicarious reinforcement paradigm. Monkeys were cued as to whether an upcoming reward would be delivered to them, another monkey, or nobody and could accept or decline the offer. As expected, all monkeys in both laboratories showed a marked preference for juice to the self, together with a reliable prosocial preference for juice to a social partner compared to juice to nobody. However, contrary to the autonomic arousal hypothesis, we found that pupils were widest in anticipation of juice to the self, moderately-sized in anticipation of juice to nobody, and narrowest in anticipation of juice to a social partner. This effect was seen across both laboratories and regardless of specific task parameters. The seemingly paradoxical pupil effect can be explained by a model in which pupil size tracks outcome salience, prosocial tendencies track outcome valence, and the relation between salience and valence is U-shaped.

animal behavior and cognition↗