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Abstract
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The mammalian brain is organized in overlapping, intercalated circuits, and an extensive body of information has focused on the maturation of sensory (visual, auditory) and motor circuits (1-3). Yet, much less is known about the maturation principles of "emotional" brain circuits, including those governing reward-, stress-, and fear-related behaviors. Evidence suggests that sensory inputs from the environment during a sensitive period in early postnatal life have important effects on emotional circuit development, just as adverse or positive images, odors, and sounds influence feelings and actions in adulthood. Disrupted operation of emotional circuits underlies mental illnesses and substance use disorders. Therefore, enhanced recognition of the principles guiding the development of these circuits is important for understanding human health.
The establishment of sensory circuits throughout development involves an initial phase of genetically and molecularly driven events, including neuronal migration and the construction of synapses. The subsequent strengthening or pruning of synapses is a network activity-dependent process that sculpts mature circuits (4). The network activity crucial to this process is, in turn, driven by circuit-specific sensory inputs (e.g., sequences of tone, light, or touch). In addition, the sensory signal-driven network activity must take place during a critical or sensitive period.
However, the execution of complex behaviors in humans and other mammals--and the computations, decisions, and emotions that contribute to such behaviors--requires additional brain circuits. These receive converging information from networks encoding andprocessing environmental signals, and from nerve projections that convey the internal state of the body (see the figure). These high-order circuits, considered "emotional" or "cognitive" according to their primary involvement in human behavior (e.g., memory may be cognitive whereas "instinct" may be emotional), adjudicate numerous streams of information to drive complex behaviors. Whereas discoveries about the structure and function of emotional circuits are increasing, their development, and specifically the influence of environmental signals on their maturation, remains poorly understood. Focusing on the influence of sensory signals early in postnatal life on emotional circuit maturation, it is proposed that unpredictable sequences of environmental signals influence emotional circuit development and refinement, promoting vulnerabilities to emotional illnesses. |