Elucidating multifinal and equifinal pathways to developmental disorders by constructing real-world neurorobotic models.

Vigorous research has been conducted to accumulate biological and theoretical knowledge about neurodevelopmental disorders, including molecular, neural, computational, and behavioral characteristics; however, these findings remain fragmentary and do not elucidate integrated mechanisms. An obstacle is the heterogeneity of developmental pathways causing clinical phenotypes. Additionally, in symptom formations, the primary causes and consequences of developmental learning processes are often indistinguishable. Herein, we review developmental neurorobotic experiments tackling problems related to the dynamic and complex properties of neurodevelopmental disorders. Specifically, we focus on neurorobotic models under predictive processing lens for the study of developmental disorders. By constructing neurorobotic models with predictive processing mechanisms of learning, perception, and action, we can simulate formations of integrated causal relationships among neurodynamical, computational, and behavioral characteristics in the robot agents while considering developmental learning processes. This framework has the potential to bind neurobiological hypotheses (excitation-inhibition imbalance and functional disconnection), computational accounts (unusual encoding of uncertainty), and clinical symptoms. Developmental neurorobotic approaches may serve as a complementary research framework for integrating fragmented knowledge and overcoming the heterogeneity of neurodevelopmental disorders.

Emergence of sensory attenuation based upon the free-energy principle.

The brain attenuates its responses to self-produced exteroceptions (e.g., we cannot tickle ourselves). Is this phenomenon, known as sensory attenuation, enabled innately, or acquired through learning? Here, our simulation study using a multimodal hierarchical recurrent neural network model, based on variational free-energy minimization, shows that a mechanism for sensory attenuation can develop through learning of two distinct types of sensorimotor experience, involving self-produced or externally produced exteroceptions. For each sensorimotor context, a particular free-energy state emerged through interaction between top-down prediction with precision and bottom-up sensory prediction error from each sensory area. The executive area in the network served as an information hub. Consequently, shifts between the two sensorimotor contexts triggered transitions from one free-energy state to another in the network via executive control, which caused shifts between attenuating and amplifying prediction-error-induced responses in the sensory areas. This study situates emergence of sensory attenuation (or self-other distinction) in development of distinct free-energy states in the dynamic hierarchical neural system.

Neural network modeling of altered facial expression recognition in autism spectrum disorders based on predictive processing framework.

The mechanism underlying the emergence of emotional categories from visual facial expression information during the developmental process is largely unknown. Therefore, this study proposes a system-level explanation for understanding the facial emotion recognition process and its alteration in autism spectrum disorder (ASD) from the perspective of predictive processing theory. Predictive processing for facial emotion recognition was implemented as a hierarchical recurrent neural network (RNN). The RNNs were trained to predict the dynamic changes of facial expression movies for six basic emotions without explicit emotion labels as a developmental learning process, and were evaluated by the performance of recognizing unseen facial expressions for the test phase. In addition, the causal relationship between the network characteristics assumed in ASD and ASD-like cognition was investigated. After the developmental learning process, emotional clusters emerged in the natural course of self-organization in higher-level neurons, even though emotional labels were not explicitly instructed. In addition, the network successfully recognized unseen test facial sequences by adjusting higher-level activity through the process of minimizing precision-weighted prediction error. In contrast, the network simulating altered intrinsic neural excitability demonstrated reduced generalization capability and impaired emotional clustering in higher-level neurons. Consistent with previous findings from human behavioral studies, an excessive precision estimation of noisy details underlies this ASD-like cognition. These results support the idea that impaired facial emotion recognition in ASD can be explained by altered predictive processing, and provide possible insight for investigating the neurophysiological basis of affective contact.

Paradoxical sensory reactivity induced by functional disconnection in a robot model of neurodevelopmental disorder.

Neurodevelopmental disorders are characterized by heterogeneous and non-specific nature of their clinical symptoms. In particular, hyper- and hypo-reactivity to sensory stimuli are diagnostic features of autism spectrum disorder and are reported across many neurodevelopmental disorders. However, computational mechanisms underlying the unusual paradoxical behaviors remain unclear. In this study, using a robot controlled by a hierarchical recurrent neural network model with predictive processing and learning mechanism, we simulated how functional disconnection altered the learning process and subsequent behavioral reactivity to environmental change. The results show that, through the learning process, long-range functional disconnection between distinct network levels could simultaneously lower the precision of sensory information and higher-level prediction. The alteration caused a robot to exhibit sensory-dominated and sensory-ignoring behaviors ascribed to sensory hyper- and hypo-reactivity, respectively. As long-range functional disconnection became more severe, a frequency shift from hyporeactivity to hyperreactivity was observed, paralleling an early sign of autism spectrum disorder. Furthermore, local functional disconnection at the level of sensory processing similarly induced hyporeactivity due to low sensory precision. These findings suggest a computational explanation for paradoxical sensory behaviors in neurodevelopmental disorders, such as coexisting hyper- and hypo-reactivity to sensory stimulus. A neurorobotics approach may be useful for bridging various levels of understanding in neurodevelopmental disorders and providing insights into mechanisms underlying complex clinical symptoms.

Homogeneous Intrinsic Neuronal Excitability Induces Overfitting to Sensory Noise: A Robot Model of Neurodevelopmental Disorder.

Neurodevelopmental disorders, including autism spectrum disorder, have been intensively investigated at the neural, cognitive, and behavioral levels, but the accumulated knowledge remains fragmented. In particular, developmental learning aspects of symptoms and interactions with the physical environment remain largely unexplored in computational modeling studies, although a leading computational theory has posited associations between psychiatric symptoms and an unusual estimation of information uncertainty (precision), which is an essential aspect of the real world and is estimated through learning processes. Here, we propose a mechanistic explanation that unifies the disparate observations via a hierarchical predictive coding and developmental learning framework, which is demonstrated in experiments using a neural network-controlled robot. The results show that, through the developmental learning process, homogeneous intrinsic neuronal excitability at the neural level induced via self-organization changes at the information processing level, such as hyper sensory precision and overfitting to sensory noise. These changes led to multifaceted alterations at the behavioral level, such as inflexibility, reduced generalization, and motor clumsiness. In addition, these behavioral alterations were accompanied by fluctuating neural activity and excessive development of synaptic connections. These findings might bridge various levels of understandings in autism spectrum and other neurodevelopmental disorders and provide insights into the disease processes underlying observed behaviors and brain activities in individual patients. This study shows the potential of neurorobotics frameworks for modeling how psychiatric disorders arise from dynamic interactions among the brain, body, and uncertain environments.

A Neurorobotics Simulation of Autistic Behavior Induced by Unusual Sensory Precision.

Recently, applying computational models developed in cognitive science to psychiatric disorders has been recognized as an essential approach for understanding cognitive mechanisms underlying psychiatric symptoms. Autism spectrum disorder is a neurodevelopmental disorder that is hypothesized to affect information processes in the brain involving the estimation of sensory precision (uncertainty), but the mechanism by which observed symptoms are generated from such abnormalities has not been thoroughly investigated. Using a humanoid robot controlled by a neural network using a precision-weighted prediction error minimization mechanism, it is suggested that both increased and decreased sensory precision could induce the behavioral rigidity characterized by resistance to change that is characteristic of autistic behavior. Specifically, decreased sensory precision caused any error signals to be disregarded, leading to invariability of the robot's intention, while increased sensory precision caused an excessive response to error signals, leading to fluctuations and subsequent fixation of intention. The results may provide a system-level explanation of mechanisms underlying different types of behavioral rigidity in autism spectrum and other psychiatric disorders. In addition, our findings suggest that symptoms caused by decreased and increased sensory precision could be distinguishable by examining the internal experience of patients and neural activity coding prediction error signals in the biological brain.