Neuromodulatory control of complex adaptive dynamics in the brain

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Abstract

How is the massive dimensionality and complexity of the microscopic constituents of the nervous system brought under sufficiently tight control so as to coordinate adaptive behaviour? A powerful means for striking this balance is to poise neurons close to the critical point of a phase transition, at which a small change in neuronal excitability can manifest a nonlinear augmentation in neuronal activity. How the brain could mediate this critical transition is a key open question in neuroscience. Here, I propose that the different arms of the ascending arousal system provide the brain with a diverse set of heterogeneous control parameters that can be used to modulate the excitability and receptivity of target neurons—in other words, to act as control parameters for mediating critical neuronal order. Through a series of worked examples, I demonstrate how the neuromodulatory arousal system can interact with the inherent topological complexity of neuronal subsystems in the brain to mediate complex adaptive behaviour.

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Situating the default-mode network along a principal gradient of macroscale cortical organization.

Daniel S. Margulies, Satrajit Ghosh, Alexandros Goulas … (2016)

Understanding how the structure of cognition arises from the topographical organization of the cortex is a primary goal in neuroscience. Previous work has described local functional gradients extending from perceptual and motor regions to cortical areas representing more abstract functions, but an overarching framework for the association between structure and function is still lacking. Here, we show that the principal gradient revealed by the decomposition of connectivity data in humans and the macaque monkey is anchored by, at one end, regions serving primary sensory/motor functions and at the other end, transmodal regions that, in humans, are known as the default-mode network (DMN). These DMN regions exhibit the greatest geodesic distance along the cortical surface-and are precisely equidistant-from primary sensory/motor morphological landmarks. The principal gradient also provides an organizing spatial framework for multiple large-scale networks and characterizes a spectrum from unimodal to heteromodal activity in a functional metaanalysis. Together, these observations provide a characterization of the topographical organization of cortex and indicate that the role of the DMN in cognition might arise from its position at one extreme of a hierarchy, allowing it to process transmodal information that is unrelated to immediate sensory input.

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An integrative theory of locus coeruleus-norepinephrine function: adaptive gain and optimal performance.

Gary Aston-Jones, Jonathan D. Cohen (2005)

Historically, the locus coeruleus-norepinephrine (LC-NE) system has been implicated in arousal, but recent findings suggest that this system plays a more complex and specific role in the control of behavior than investigators previously thought. We review neurophysiological and modeling studies in monkey that support a new theory of LC-NE function. LC neurons exhibit two modes of activity, phasic and tonic. Phasic LC activation is driven by the outcome of task-related decision processes and is proposed to facilitate ensuing behaviors and to help optimize task performance (exploitation). When utility in the task wanes, LC neurons exhibit a tonic activity mode, associated with disengagement from the current task and a search for alternative behaviors (exploration). Monkey LC receives prominent, direct inputs from the anterior cingulate (ACC) and orbitofrontal cortices (OFC), both of which are thought to monitor task-related utility. We propose that these frontal areas produce the above patterns of LC activity to optimize utility on both short and long timescales.

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An anatomically comprehensive atlas of the adult human brain transcriptome.

Michael Hawrylycz, Ed Lein, Angela Guillozet-Bongaarts … (2012)

Neuroanatomically precise, genome-wide maps of transcript distributions are critical resources to complement genomic sequence data and to correlate functional and genetic brain architecture. Here we describe the generation and analysis of a transcriptional atlas of the adult human brain, comprising extensive histological analysis and comprehensive microarray profiling of ∼900 neuroanatomically precise subdivisions in two individuals. Transcriptional regulation varies enormously by anatomical location, with different regions and their constituent cell types displaying robust molecular signatures that are highly conserved between individuals. Analysis of differential gene expression and gene co-expression relationships demonstrates that brain-wide variation strongly reflects the distributions of major cell classes such as neurons, oligodendrocytes, astrocytes and microglia. Local neighbourhood relationships between fine anatomical subdivisions are associated with discrete neuronal subtypes and genes involved with synaptic transmission. The neocortex displays a relatively homogeneous transcriptional pattern, but with distinct features associated selectively with primary sensorimotor cortices and with enriched frontal lobe expression. Notably, the spatial topography of the neocortex is strongly reflected in its molecular topography-the closer two cortical regions, the more similar their transcriptomes. This freely accessible online data resource forms a high-resolution transcriptional baseline for neurogenetic studies of normal and abnormal human brain function.