Communication, the effective delivery of information, is fundamental to life across all scales and species. Nervous systems (by necessity) may be most specifically adapted among biological tissues for high rate and complexity of information transmitted, and thus, the properties of neural tissue and principles of its organization into circuits may illuminate capabilities and limitations of biological communication. Here, we consider recent developments in tools for studying neural circuits with particular attention to defining neuronal cell types by input and output information streams—i.e., by how they communicate. Complementing approaches that define cell types by virtue of genetic promoter/enhancer properties, this communication-based approach to defining cell types operationally by input/output (I/O) relationships links structure and function, resolves difficulties associated with single-genetic-feature definitions, leverages technology for observing and testing significance of precisely these I/O relationships in intact brains, and maps onto processes through which behavior may be adapted during development, experience, and evolution.Nervous systems are designed for communication over many scales, beginning at the most fundamental level shared by all cellular systems in biology, in which communication occurs via protein-protein interactions, movement of second messengers within cells, and local release and detection of diffusible transmitters between cells. Nervous systems become clearly unique in their communication properties only at the tissue and organ level, in which billions of cells may work together as an intricately organized, interconnected circuit. It is through the organization of cells into these neural circuits that the brain supports the vast diversity of animal behavior, up to and including human consciousness, cognition, and emotion. Neural circuits are both extremely complex and exquisitely specific, and the connectivity motifs used to build these circuits vary widely even within a single organism. Contrast the mammalian cerebellar granule neuron, which may receive only five mossy fiber inputs (Llinas et al., 2004) with the mammalian cortical pyramidal neuron, which receives thousands of inputs from a broad array of cortical and subcortical brain regions (Ballesteros-Ya´ n˜ ez et al., 2006). As with inputs, output structuring of neuronal types is also highly diverse, with a broad range of numbers and distributions of both local downstream neurons and distant postsynaptic partners across the nervous system. Indeed, each neuron type might be viewed as a distinct elemental device, definable in part by how it communicates via receiving, processing, and disseminating information. Understanding communication in the nervous system will require analyzing the input/output organization of these elements within larger neural circuits, observing the actual operation of these elements during behavior, and testing hypotheses built on this knowledge with model-guided perturbations targeted to these elements to determine the behaviorally relevant dynamics of information flow and processing. Given the fundamental necessity of cell-cell communication for brain function, neuroscientists have long devoted substantial effort to developing and deploying technologies for exploring the structure and function of brain communication networks. Although many decades of neuroanatomical research have provided foundational principles underlying neural circuit organization, much remains to be discovered, and opportunities for discovery are particularly abundant at the borders between communication scales. Recent technological developments are indeed beginning to allow neuroscientists to connect neuronal circuit architecture and activity information across different scales and modalities. These methods are advancing the understanding of circuits in behaviorally relevant contexts, while at the same time heightening the need for cell typology that is more tightly linked to function, in order to define the cellular properties that are most relevant for nervous system operation. In this primer, we focus on currently available and rapidly evolving technologies for such structural and functional circuit-level analysis—with attention to both opportunities and limitations—and highlight the concept of the input/output (I/O)-defined circuit element (IODE) as a basic and recent experimentally tractable building block for the study and understanding of nervous system communication across scales.
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Communication in Neural Circuits: Tools, Opportunities, and Challenges: Cell