Modular Neuronal Assemblies Embodied in a Closed-Loop Environment: Toward Future Integration of Brains and Machines

Behaviors, from simple to most complex, require a two-way interaction with the environment and the contribution of different brain areas depending on the orchestrated activation of neuronal assemblies. In this work we present a new hybrid neuro-robotic architecture based on a neural controller bi-directionally connected to a virtual robot implementing a Braitenberg vehicle aimed at avoiding obstacles. The robot is characterized by proximity sensors and wheels, allowing it to navigate into a circular arena with obstacles of different sizes. As neural controller, we used hippocampal cultures dissociated from embryonic rats and kept alive over Micro Electrode Arrays (MEAs) for 3–8 weeks. The developed software architecture guarantees a bi-directional exchange of information between the natural and the artificial part by means of simple linear coding/decoding schemes. We used two different kinds of experimental preparation: “random” and “modular” populations. In the second case, the confinement was assured by a polydimethylsiloxane (PDMS) mask placed over the surface of the MEA device, thus defining two populations interconnected via specific microchannels. The main results of our study are: (i) neuronal cultures can be successfully interfaced to an artificial agent; (ii) modular networks show a different dynamics with respect to random culture, both in terms of spontaneous and evoked electrophysiological patterns; (iii) the robot performs better if a reinforcement learning paradigm (i.e., a tetanic stimulation delivered to the network following each collision) is activated, regardless of the modularity of the culture; (iv) the robot controlled by the modular network further enhances its capabilities in avoiding obstacles during the short-term plasticity trial. The developed paradigm offers a new framework for studying, in simplified model systems, neuro-artificial bi-directional interfaces for the development of new strategies for brain-machine interaction.