scholarly journals Scaffolding layered control architectures through constraint closure: insights into brain evolution and development

Author(s):  
Stuart P. Wilson ◽  
Tony J. Prescott

The functional organization of the mammalian brain can be considered to form a layered control architecture, but how this complex system has emerged through evolution and is constructed during development remains a puzzle. Here we consider brain organization through the framework of constraint closure, viewed as a general characteristic of living systems, that they are composed of multiple sub-systems that constrain each other at different timescales. We do so by developing a new formalism for constraint closure, inspired by a previous model showing how within-lifetime dynamics can constrain between-lifetime dynamics, and we demonstrate how this interaction can be generalized to multi-layered systems. Through this model, we consider brain organization in the context of two major examples of constraint closure—physiological regulation and visual orienting. Our analysis draws attention to the capacity of layered brain architectures to scaffold themselves across multiple timescales, including the ability of cortical processes to constrain the evolution of sub-cortical processes, and of the latter to constrain the space in which cortical systems self-organize and refine themselves. This article is part of the theme issue ‘Systems neuroscience through the lens of evolutionary theory’.

2017 ◽  
Vol 7 (1) ◽  
Author(s):  
Serena Bovetti ◽  
Claudio Moretti ◽  
Stefano Zucca ◽  
Marco Dal Maschio ◽  
Paolo Bonifazi ◽  
...  

Abstract Genetically encoded calcium indicators and optogenetic actuators can report and manipulate the activity of specific neuronal populations. However, applying imaging and optogenetics simultaneously has been difficult to establish in the mammalian brain, even though combining the techniques would provide a powerful approach to reveal the functional organization of neural circuits. Here, we developed a technique based on patterned two-photon illumination to allow fast scanless imaging of GCaMP6 signals in the intact mouse brain at the same time as single-photon optogenetic inhibition with Archaerhodopsin. Using combined imaging and electrophysiological recording, we demonstrate that single and short bursts of action potentials in pyramidal neurons can be detected in the scanless modality at acquisition frequencies up to 1 kHz. Moreover, we demonstrate that our system strongly reduces the artifacts in the fluorescence detection that are induced by single-photon optogenetic illumination. Finally, we validated our technique investigating the role of parvalbumin-positive (PV) interneurons in the control of spontaneous cortical dynamics. Monitoring the activity of cellular populations on a precise spatiotemporal scale while manipulating neuronal activity with optogenetics provides a powerful tool to causally elucidate the cellular mechanisms underlying circuit function in the intact mammalian brain.


2020 ◽  
Vol 117 (19) ◽  
pp. 10554-10564 ◽  
Author(s):  
Annalisa Paolino ◽  
Laura R. Fenlon ◽  
Peter Kozulin ◽  
Elizabeth Haines ◽  
Jonathan W. C. Lim ◽  
...  

A unique combination of transcription factor expression and projection neuron identity demarcates each layer of the cerebral cortex. During mouse and human cortical development, the transcription factor CTIP2 specifies neurons that project subcerebrally, while SATB2 specifies neuronal projections via the corpus callosum, a large axon tract connecting the two neocortical hemispheres that emerged exclusively in eutherian mammals. Marsupials comprise the sister taxon of eutherians but do not have a corpus callosum; their intercortical commissural neurons instead project via the anterior commissure, similar to egg-laying monotreme mammals. It remains unknown whether divergent transcriptional networks underlie these cortical wiring differences. Here, we combine birth-dating analysis, retrograde tracing, gene overexpression and knockdown, and axonal quantification to compare the functions of CTIP2 and SATB2 in neocortical development, between the eutherian mouse and the marsupial fat-tailed dunnart. We demonstrate a striking degree of structural and functional homology, whereby CTIP2 or SATB2 of either species is sufficient to promote a subcerebral or commissural fate, respectively. Remarkably, we reveal a substantial delay in the onset of developmental SATB2 expression in mice as compared to the equivalent stage in dunnarts, with premature SATB2 overexpression in mice to match that of dunnarts resulting in a marsupial-like projection fate via the anterior commissure. Our results suggest that small alterations in the timing of regulatory gene expression may underlie interspecies differences in neuronal projection fate specification.


2021 ◽  
Vol 11 (1) ◽  
Author(s):  
Marija Markicevic ◽  
Iurii Savvateev ◽  
Christina Grimm ◽  
Valerio Zerbi

AbstractIn the past decade, the idea that single populations of neurons support cognition and behavior has gradually given way to the realization that connectivity matters and that complex behavior results from interactions between remote yet anatomically connected areas that form specialized networks. In parallel, innovation in brain imaging techniques has led to the availability of a broad set of imaging tools to characterize the functional organization of complex networks. However, each of these tools poses significant technical challenges and faces limitations, which require careful consideration of their underlying anatomical, physiological, and physical specificity. In this review, we focus on emerging methods for measuring spontaneous or evoked activity in the brain. We discuss methods that can measure large-scale brain activity (directly or indirectly) with a relatively high temporal resolution, from milliseconds to seconds. We further focus on methods designed for studying the mammalian brain in preclinical models, specifically in mice and rats. This field has seen a great deal of innovation in recent years, facilitated by concomitant innovation in gene-editing techniques and the possibility of more invasive recordings. This review aims to give an overview of currently available preclinical imaging methods and an outlook on future developments. This information is suitable for educational purposes and for assisting scientists in choosing the appropriate method for their own research question.


2014 ◽  
Vol 369 (1635) ◽  
pp. 20120511 ◽  
Author(s):  
Edvard I. Moser ◽  
May-Britt Moser ◽  
Yasser Roudi

One of the major breakthroughs in neuroscience is the emerging understanding of how signals from the external environment are extracted and represented in the primary sensory cortices of the mammalian brain. The operational principles of the rest of the cortex, however, have essentially remained in the dark. The discovery of grid cells, and their functional organization, opens the door to some of the first insights into the workings of the association cortices, at a stage of neural processing where firing properties are shaped not primarily by the nature of incoming sensory signals but rather by internal self-organizing principles. Grid cells are place-modulated neurons whose firing locations define a periodic triangular array overlaid on the entire space available to a moving animal. The unclouded firing pattern of these cells is rare within the association cortices. In this paper, we shall review recent advances in our understanding of the mechanisms of grid-cell formation which suggest that the pattern originates by competitive network interactions, and we shall relate these ideas to new insights regarding the organization of grid cells into functionally segregated modules.


2010 ◽  
Vol 12 (4) ◽  
pp. 463-470 ◽  

Continuing to discover how the brain works is one of the great challenges ahead of us. Although understanding the brain anatomy and its functional organization provided a first and indispensable foundation, it became clear that a static view was insufficient. To understand the complexity of neuronal communication, it is necessary to examine the chemical nature of the neurotransmission and, using the example of the acetylcholine receptors, follow the different layers of networks that can be distinguished. The natural alkaloid nicotine contained in tobacco leaves acts as an agonist with a subclass of acetylcholine receptors, and provides an interesting tool to approach brain functions. Analysis of the nicotinic acetylcholine receptors, which are ligand gated channels, revealed that these receptors are expressed at different critical locations on the neurons including the synaptic boutons, neurites, cell bodies, and even on the axons. These receptors can modulate the activity at the microcircuit synaptic level, in the cell processing of information, and, by acting on the velocity of action potential, the synchrony of communication between brain areas. These actions at multiple levels of brain organization provide an example of the complexity of brain neurocircuitry and an illustration of the relevance of this knowledge for psychiatry.


2017 ◽  
Author(s):  
Ella Striem-Amit ◽  
Gilles Vannuscorps ◽  
Alfonso Caramazza

SummaryWhat forces direct brain organization and its plasticity? When a brain region is deprived of its input would this region reorganize based on compensation for the disability and experience, or would strong limitations of brain structure limit its plasticity? People born without hands activate their sensorimotor hand region while moving body parts used to compensate for this ability (e.g. their feet). This has been taken to suggest a neural organization based on functions, such as performing manual-like dexterous actions, rather than on body parts. Here we test the selectivity for functionally-compensatory body parts in the sensorimotor cortex of people born without hands. Despite clear compensatory foot use, the sensorimotor hand area in the dysplasic subjects showed preference for body parts whose cortical territory is close to the hand area, but which are not compensatorily used as effectors. This suggests that function-based organization, originally proposed for congenital blindness and deafness, does not apply to cases of the primary sensorimotor cortex deprivation in dysplasia. This is consistent with the idea that experience-independent functional specialization occurs at relatively high levels of representation. Indeed, increased and selective foot movement preference in the dysplasics was found in the association cortex, in the inferior parietal lobule. Furthermore, it stresses the roles of neuroanatomical constraints such as topographical proximity and connectivity in determining the functional development of brain regions. These findings reveal limitations to brain plasticity and to the role of experience in shaping the functional organization of the brain.Significance StatementWhat determines the role of brain regions, and their plasticity when typical inputs or experience is not provided? To what extent can extreme compensatory use affect brain organization? We tested the functional reorganization of the primary sensorimotor cortex hand area in people born without hands, who use their feet for every-day tasks. We found that it is preferentially activated by close-by body-parts which cannot serve as effectors, and not by the feet. In contrast, foot-selective compensatory plasticity was found in the association cortex, in an area involved in tool use. This shows limitations of compensatory plasticity and experience in modifying brain organization of early topographical cortex, as compared to association cortices where function-based organization is the driving factor.ClassificationBiological Sciences\Neuroscience


2019 ◽  
Vol 26 (2) ◽  
pp. 117-133 ◽  
Author(s):  
Corey Horien ◽  
Abigail S. Greene ◽  
R. Todd Constable ◽  
Dustin Scheinost

Functional magnetic resonance imaging has proved to be a powerful tool to characterize spatiotemporal patterns of human brain activity. Analysis methods broadly fall into two camps: those summarizing properties of a region and those measuring interactions among regions. Here we pose an unappreciated question in the field: What are the strengths and limitations of each approach to study fundamental neural processes? We explore the relative utility of region- and connection-based measures in the context of three topics of interest: neurobiological relevance, brain-behavior relationships, and individual differences in brain organization. In each section, we offer illustrative examples. We hope that this discussion offers a novel and useful framework to support efforts to better understand the macroscale functional organization of the brain and how it relates to behavior.


2016 ◽  
Vol 283 (1838) ◽  
pp. 20160433 ◽  
Author(s):  
Stephen H. Montgomery ◽  
Nicholas I. Mundy ◽  
Robert A. Barton

Phenotypic traits are products of two processes: evolution and development. But how do these processes combine to produce integrated phenotypes? Comparative studies identify consistent patterns of covariation, or allometries, between brain and body size, and between brain components, indicating the presence of significant constraints limiting independent evolution of separate parts. These constraints are poorly understood, but in principle could be either developmental or functional. The developmental constraints hypothesis suggests that individual components (brain and body size, or individual brain components) tend to evolve together because natural selection operates on relatively simple developmental mechanisms that affect the growth of all parts in a concerted manner. The functional constraints hypothesis suggests that correlated change reflects the action of selection on distributed functional systems connecting the different sub-components, predicting more complex patterns of mosaic change at the level of the functional systems and more complex genetic and developmental mechanisms. These hypotheses are not mutually exclusive but make different predictions. We review recent genetic and neurodevelopmental evidence, concluding that functional rather than developmental constraints are the main cause of the observed patterns.


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