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      Cerebral hierarchies: predictive processing, precision and the pulvinar

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          Abstract

          This paper considers neuronal architectures from a computational perspective and asks what aspects of neuroanatomy and neurophysiology can be disclosed by the nature of neuronal computations? In particular, we extend current formulations of the brain as an organ of inference—based upon hierarchical predictive coding—and consider how these inferences are orchestrated. In other words, what would the brain require to dynamically coordinate and contextualize its message passing to optimize its computational goals? The answer that emerges rests on the delicate (modulatory) gain control of neuronal populations that select and coordinate (prediction error) signals that ascend cortical hierarchies. This is important because it speaks to a hierarchical anatomy of extrinsic (between region) connections that form two distinct classes, namely a class of driving (first-order) connections that are concerned with encoding the content of neuronal representations and a class of modulatory (second-order) connections that establish context—in the form of the salience or precision ascribed to content. We explore the implications of this distinction from a formal perspective (using simulations of feature–ground segregation) and consider the neurobiological substrates of the ensuing precision-engineered dynamics, with a special focus on the pulvinar and attention.

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          A free energy principle for the brain.

          By formulating Helmholtz's ideas about perception, in terms of modern-day theories, one arrives at a model of perceptual inference and learning that can explain a remarkable range of neurobiological facts: using constructs from statistical physics, the problems of inferring the causes of sensory input and learning the causal structure of their generation can be resolved using exactly the same principles. Furthermore, inference and learning can proceed in a biologically plausible fashion. The ensuing scheme rests on Empirical Bayes and hierarchical models of how sensory input is caused. The use of hierarchical models enables the brain to construct prior expectations in a dynamic and context-sensitive fashion. This scheme provides a principled way to understand many aspects of cortical organisation and responses. In this paper, we show these perceptual processes are just one aspect of emergent behaviours of systems that conform to a free energy principle. The free energy considered here measures the difference between the probability distribution of environmental quantities that act on the system and an arbitrary distribution encoded by its configuration. The system can minimise free energy by changing its configuration to affect the way it samples the environment or change the distribution it encodes. These changes correspond to action and perception respectively and lead to an adaptive exchange with the environment that is characteristic of biological systems. This treatment assumes that the system's state and structure encode an implicit and probabilistic model of the environment. We will look at the models entailed by the brain and how minimisation of its free energy can explain its dynamics and structure.
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            The Helmholtz machine.

            Discovering the structure inherent in a set of patterns is a fundamental aim of statistical inference or learning. One fruitful approach is to build a parameterized stochastic generative model, independent draws from which are likely to produce the patterns. For all but the simplest generative models, each pattern can be generated in exponentially many ways. It is thus intractable to adjust the parameters to maximize the probability of the observed patterns. We describe a way of finessing this combinatorial explosion by maximizing an easily computed lower bound on the probability of the observations. Our method can be viewed as a form of hierarchical self-supervised learning that may relate to the function of bottom-up and top-down cortical processing pathways.
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              Cortical mechanisms of action selection: the affordance competition hypothesis.

              Paul Cisek (2007)
              At every moment, the natural world presents animals with two fundamental pragmatic problems: selection between actions that are currently possible and specification of the parameters or metrics of those actions. It is commonly suggested that the brain addresses these by first constructing representations of the world on which to build knowledge and make a decision, and then by computing and executing an action plan. However, neurophysiological data argue against this serial viewpoint. In contrast, it is proposed here that the brain processes sensory information to specify, in parallel, several potential actions that are currently available. These potential actions compete against each other for further processing, while information is collected to bias this competition until a single response is selected. The hypothesis suggests that the dorsal visual system specifies actions which compete against each other within the fronto-parietal cortex, while a variety of biasing influences are provided by prefrontal regions and the basal ganglia. A computational model is described, which illustrates how this competition may take place in the cerebral cortex. Simulations of the model capture qualitative features of neurophysiological data and reproduce various behavioural phenomena.
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                Author and article information

                Journal
                Philos Trans R Soc Lond B Biol Sci
                Philos. Trans. R. Soc. Lond., B, Biol. Sci
                RSTB
                royptb
                Philosophical Transactions of the Royal Society B: Biological Sciences
                The Royal Society
                0962-8436
                1471-2970
                19 May 2015
                19 May 2015
                : 370
                : 1668 , Theme issue ‘Cerebral cartography: a vision of its future’ compiled and edited by Semir Zeki
                : 20140169
                Affiliations
                [1 ]School of Psychology, Sackler Centre for Consciousness Science, University of Sussex , Brighton BN1 9QH, UK
                [2 ]Precursory Research for Embryonic Science and Technology, Japan Science and Technology Agency , Saitama 332-0012, Japan
                [3 ]Systems Neuroscience, Human Technology Research Institute, National Institute of Advanced Industrial Science and Technology , Tsukuba 305-8568, Japan
                [4 ]UCL Institute of Ophthalmology , London EC1V 9EL, UK
                [5 ]Wellcome Trust Centre for Neuroimaging, Institute of Neurology, UCL , London WC1 3BG, UK
                Author notes

                One contribution of 11 to a theme issue ‘ Cerebral cartography: a vision of its future’.

                Article
                rstb20140169
                10.1098/rstb.2014.0169
                4387510
                25823866
                0f3882ad-0a6b-4963-8963-2deced4f7724

                © 2015 The Authors. Published by the Royal Society under the terms of the Creative Commons Attribution License http://creativecommons.org/licenses/by/4.0/, which permits unrestricted use, provided the original author and source are credited.

                History
                : 12 November 2014
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                May 19, 2015

                Philosophy of science
                neuronal computational,attention,predictive coding,precision,neuromodulation,pulvinar

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