Characterizing functional hippocampal pathways in a brain-based device as it solves a spatial memory task

Abstract

Analyzing neural dynamics underlying complex behavior is a major challenge in systems neurobiology. To meet this challenge through computational neuroscience, we have constructed a brain-based device (Darwin X) that interacts with a real environment, and whose behavior is guided by a simulated nervous system incorporating detailed aspects of the anatomy and physiology of the hippocampus and its surrounding regions. Darwin X integrates cues from its environment to solve a spatial memory task. Placespecific units, similar to place cells in the rodent, emerged by integrating visual and self-movement cues during exploration without prior assumptions in the model about environmental inputs. Because synthetic neural modeling using brain-based devices allows recording from all elements of the simulated nervous system during behavior, we were able to identify different functional hippocampal pathways. We did this by tracing back from reference neuronal units in the CA1 region of the simulated hippocampus to all of the synaptically connected units that were coactive during a particular exploratory behavior. Our analysis identified a number of different functional pathways within the simulated hippocampus that incorporate either the perforant path or the trisynaptic loop. Place fields, which were activated by the trisynaptic circuit, tended to be more selective and informative. However, place units that were activated by the perforant path were prevalent in the model and were crucial for generating appropriate exploratory behavior. Thus, in the model, different functional pathways influence place field activity and, hence, behavior during navigation.A nalyzing the complexities of neural dynamics underlying behavior is a difficult task for systems neurobiologists. A number of factors contribute to this complexity: the variability of behavior, the multilevel nature and nonlinearity of neural interactions, and the large number of neurons in different functioning brain regions. These factors challenge the design of experimental approaches as well as the construction of computational models. For this reason, we have constructed brainbased devices (BBDs) whose behavior in a real world environment is guided by a simulated nervous system based on features of vertebrate neuroanatomy and neurophysiology. The power of this approach is that it allows simultaneous recording of the state and interactions of all components of the simulated nervous system at all levels during a behavioral task in the real world. Here, we describe a functional analysis of neural patterns in Darwin X, a BBD incorporating aspects of the detailed anatomy and physiology of the hippocampus and its surrounding regions (1). Over the last 12 years, we have successfully constructed BBDs to test theories of the nervous system having to do with perceptual categorization, primary and secondary conditioning, visual binding, and texture discrimination (2-6).Darwin X can integrate cues from its environment and provide flexible navigation solutions to spatial memory task...

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