Anthropomorphizing without Social Cues Requires the Basolateral Amygdala

Anthropomorphism, the attribution of distinctively human mental characteristics to nonhuman animals and objects, illustrates the human propensity for extending social cognition beyond typical social targets. Yet, its processing components remain challenging to study because they are typically all engaged simultaneously. Across one pilot study and one focal study, we tested three rare people with basolateral amygdala lesions to dissociate two specific processing components: those triggered by attention to social cues (e.g., seeing a face) and those triggered by endogenous semantic knowledge (e.g., imbuing a machine with animacy). A pilot study demonstrated that, like neurologically intact control group participants, the three amygdala-damaged participants produced anthropomorphic descriptions for highly socially salient stimuli but not for stimuli lacking clear social cues. A focal study found that the three amygdala participants could anthropomorphize animate and living entities normally, but anthropomorphized inanimate stimuli less than control participants. Yet, amygdala participants could anthropomorphize across all stimuli when explicitly questioned, demonstrating that the ability to make social attributions as such is intact. Our findings suggest that the amygdala contributes to how we anthropomorphize stimuli that are not explicitly social

Anthropomorphizing without Social Cues Requires the Basolateral Amygdala

Anthropomorphism, the attribution of distinctively human mental characteristics to nonhuman animals and objects, illustrates the human propensity for extending social cognition beyond typical social targets. Yet, its processing components remain challenging to study because they are typically all engaged simultaneously. Across one pilot study and one focal study, we tested three rare people with basolateral amygdala lesions to dissociate two specific processing components: those triggered by attention to social cues (e.g., seeing a face) and those triggered by endogenous semantic knowledge (e.g., imbuing a machine with animacy). A pilot study demonstrated that, like neurologically intact control group participants, the three amygdala-damaged participants produced anthropomorphic descriptions for highly socially salient stimuli but not for stimuli lacking clear social cues. A focal study found that the three amygdala participants could anthropomorphize animate and living entities normally, but anthropomorphized inanimate stimuli less than control participants. Yet, amygdala participants could anthropomorphize across all stimuli when explicitly questioned, demonstrating that the ability to make social attributions as such is intact. Our findings suggest that the amygdala contributes to how we anthropomorphize stimuli that are not explicitly social

Amygdala lesions do not compromise the cortical network for false-belief reasoning

The amygdala plays an integral role in human social cognition and behavior, with clear links to emotion recognition, trust judgments, anthropomorphization, and psychiatric disorders ranging from social phobia to autism. A central feature of human social cognition is a theory-of-mind (ToM) that enables the representation other people's mental states as distinct from one's own. Numerous neuroimaging studies of the best studied use of ToM—false-belief reasoning—suggest that it relies on a specific cortical network; moreover, the amygdala is structurally and functionally connected with many components of this cortical network. It remains unknown whether the cortical implementation of any form of ToM depends on amygdala function. Here we investigated this question directly by conducting functional MRI on two patients with rare bilateral amygdala lesions while they performed a neuroimaging protocol standardized for measuring cortical activity associated with false-belief reasoning. We compared patient responses with those of two healthy comparison groups that included 480 adults. Based on both univariate and multivariate comparisons, neither patient showed any evidence of atypical cortical activity or any evidence of atypical behavioral performance; moreover, this pattern of typical cortical and behavioral response was replicated for both patients in a follow-up session. These findings argue that the amygdala is not necessary for the cortical implementation of ToM in adulthood and suggest a reevaluation of the role of the amygdala and its cortical interactions in human social cognition

Social cognition in the age of human–robot interaction

Artificial intelligence advances have led to robots endowed with increasingly sophisticated social abilities. These machines speak to our innate desire to perceive social cues in the environment, as well as the promise of robots enhancing our daily lives. However, a strong mismatch still exists between our expectations and the reality of social robots. We argue that careful delineation of the neurocognitive mechanisms supporting human–robot interaction will enable us to gather insights critical for optimising social encounters between humans and robots. To achieve this, the field must incorporate human neuroscience tools including mobile neuroimaging to explore long-term, embodied human–robot interaction in situ. New analytical neuroimaging approaches will enable characterisation of social cognition representations on a finer scale using sensitive and appropriate categorical comparisons (human, animal, tool, or object). The future of social robotics is undeniably exciting, and insights from human neuroscience research will bring us closer to interacting and collaborating with socially sophisticated robots

A Framework for Studying Emotions across Species

Since the 19th century, there has been disagreement over the fundamental question of whether “emotions” are cause or consequence of their associated behaviors. This question of causation is most directly addressable in genetically tractable model organisms, including invertebrates such as Drosophila. Yet there is ongoing debate about whether such species even have “emotions,” as emotions are typically defined with reference to human behavior and neuroanatomy. Here, we argue that emotional behaviors are a class of behaviors that express internal emotion states. These emotion states exhibit certain general functional and adaptive properties that apply across any specific human emotions like fear or anger, as well as across phylogeny. These general properties, which can be thought of as “emotion primitives,” can be modeled and studied in evolutionarily distant model organisms, allowing functional dissection of their mechanistic bases and tests of their causal relationships to behavior. More generally, our approach not only aims at better integration of such studies in model organisms with studies of emotion in humans, but also suggests a revision of how emotion should be operationalized within psychology and psychiatry

Loving Objects: Can autism explain objectophilia?

Objectophilia (also known as Objectum-Sexuality) involves romantic and sexual attraction to specific objects. Objectophiles often develop deep and enduring emotional, romantic, and sexual relations with specific inanimate (concrete or abstract) objects such as trains, bridges, cars, or words. . The determinants of objectophilia are poorly understood. The aim of this paper is to examine the determining factors of objectophilia. We examine four hypotheses about the determinants of objectophilia (pertaining to fetishism, synesthesia, cross-modal mental imagery, and autism) and argue that the most likely determining factors of objectophilia are the social and non-social features of autism. Future studies on the determinants of objectophilia could enhance our understanding and potentially lessen the marginalization experienced by objectophiles

The social brain in psychiatric and neurological disorders

Psychiatric and neurological disorders have historically provided key insights into the structure-function relationships that subserve human social cognition and behavior, informing the concept of the 'social brain'. In this review, we take stock of the current status of this concept, retaining a focus on disorders that impact social behavior. We discuss how the social brain, social cognition, and social behavior are interdependent, and emphasize the important role of development and compensation. We suggest that the social brain, and its dysfunction and recovery, must be understood not in terms of specific structures, but rather in terms of their interaction in large-scale networks

The role of the amygdala in emotional memories:a multidisciplinary approach

This thesis investigates the role of the amygdala for the establishment of fear memories with a multidisciplinary approach, including behavioural, psychopharmacological, genetic, molecular, and electrophysiological techniques in rats or mice, under healthy or pathological conditions. This research program aims to shed light on the acquisition and storage of emotional memories in the amygdala and closely interconnected brain areas. In one line of experiments, the molecular mechanisms leading to the establishment of fear memory traces in the amygdala were investigated. For this purpose, the functional role of the polysialylated neural cell adhesion molecule PSA-NCAM, expressed in the synaptic junction, was assessed in the amygdala – and also prefrontal cortex and hippocampus – with psychopharmacological and genetic approaches and tasks that strongly rely on these brain areas. Two lines of studies were followed: 1) amygdala-targeted cleavage and enhancement of PSA-NCAM in rats and 2) general cleavage of PSA-NCAM throughout the brain using genetically modified mice. Taken together, both approaches show that amygdaloid PSA-NCAM plays no role in the acquisition and storage of fear memories, but is rather involved in their extinction. Furthermore, the results confirm the importance of PSA-NCAM in hippocampus mediated learning and for the first time show that prefrontal cortex mediated learning depends on PSA-NCAM. These results suggest that PSA-NCAM is selectively involved in some, but not all, synaptic plasticity processes in the brain. In another line of experiments, the valproic acid (VPA) animal model of autism was used to investigate a possible contribution of the amygdala towards the autistic pathology. VPA was injected once at a specific time point during gestation, the time of neural tube closure. The offspring of such treated rats were first characterized in a broad set of behavioural tasks. It was found that VPA-treated offspring exhibited very specific behavioural anomalies closely resembling autistic symptomotology, such as impaired social interaction, exploration and recognition, enhanced repetitive behaviours, impaired sensorimotor gating and increased anxiety, while other behavioural parameters were left unharmed. Once the validity of the model was established, amygdala functionality was assessed. The results demonstrated that VPA-treated offspring exhibited highly enhanced conditioned fear memories, which generalized to other stimuli and were resistant to extinction. Electrophysiological in vitro recordings in the amygdala revealed hyper-reactivity towards stimulation and enhanced activity-induced synaptic plasticity. These results imply that enhanced activity and plasticity in the amygdala may underlie the exaggerated fear memories. Furthermore it is suggested in this thesis that a hyper-reactive amygdala may underlie some of the most basic symptoms observed in autism: reduced social interactions and resistance to rehabilitation

Perceiving Sociable Technology: Exploring the Role of Anthropomorphism and Agency Perception on Human-Computer Interaction (HCI)

With the arrival of personal assistants and other AI-enabled autonomous technologies, social interactions with smart devices have become a part of our daily lives. Therefore, it becomes increasingly important to understand how these social interactions emerge, and why users appear to be influenced by them. For this reason, I explore questions on what the antecedents and consequences of this phenomenon, known as anthropomorphism, are as described in the extant literature from fields ranging from information systems to social neuroscience. I critically analyze those empirical studies directly measuring anthropomorphism and those referring to it without a corresponding measurement. Through a grounded theory approach, I identify common themes and use them to develop models for the antecedents and consequences of anthropomorphism. The results suggest anthropomorphism possesses both conscious and non-conscious components with varying implications. While conscious attributions are shown to vary based on individual differences, non-conscious attributions emerge whenever a technology exhibits apparent reasoning such as through non-verbal behavior like peer-to-peer mirroring or verbal paralinguistic and backchanneling cues. Anthropomorphism has been shown to affect users’ self-perceptions, perceptions of the technology, how users interact with the technology, and the users’ performance. Examples include changes in a users’ trust on the technology, conformity effects, bonding, and displays of empathy. I argue these effects emerge from changes in users’ perceived agency, and their self- and social- identity similarly to interactions between humans. Afterwards, I critically examine current theories on anthropomorphism and present propositions about its nature based on the results of the empirical literature. Subsequently, I introduce a two-factor model of anthropomorphism that proposes how an individual anthropomorphizes a technology is dependent on how the technology was initially perceived (top-down and rational or bottom-up and automatic), and whether it exhibits a capacity for agency or experience. I propose that where a technology lays along this spectrum determines how individuals relates to it, creating shared agency effects, or changing the users’ social identity. For this reason, anthropomorphism is a powerful tool that can be leveraged to support future interactions with smart technologies

Nature and source of animal spontaneous behaviors: Insights from psychobehavioral development and neuronal population dynamics in mice

Awake animals switch between different behavioral states irregularly even in a homogenous and steady environment, especially obvious outside from any behavioral task when they are free to voluntarily behave. These irregular but structured patterns have been taken as a representation of internal states such as emotion, and are believed to represent underlying background brain activity and its dynamics. To date, the nature and source of animal spontaneous behaviors remain as a major conceptual challenge to academia, due to the lack of approaches to systematically and quantitatively examine this fundamental process. To achieve insights about the neural substrate of animal spontaneous behaviors, the research was conducted in two directions: (i) To interpret previously challenging and inconclusive behavioral development by re-evaluating spontaneous behaviors that represent emotionality, centered on the study of PTSD (post-traumatic stress disorder)-like internal psychological development in laboratory mice; (ii) To demonstrate a driving and control principle explaining fine-scale and global observations of neuronal and behavioral dynamics in spontaneously behaving mice, by two-photon calcium imaging of neuronal populations across cerebral cortical layers and areas. The results from these investigations provide the first system-level view of experimentally disentangled components, processes, and determinants explaining the nature and source of animal spontaneous behaviors.Okinawa Institute of Science and Technology Graduate Universit