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      Hierarchical Models in the Brain

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      PLoS Computational Biology
      Public Library of Science

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          Abstract

          This paper describes a general model that subsumes many parametric models for continuous data. The model comprises hidden layers of state-space or dynamic causal models, arranged so that the output of one provides input to another. The ensuing hierarchy furnishes a model for many types of data, of arbitrary complexity. Special cases range from the general linear model for static data to generalised convolution models, with system noise, for nonlinear time-series analysis. Crucially, all of these models can be inverted using exactly the same scheme, namely, dynamic expectation maximization. This means that a single model and optimisation scheme can be used to invert a wide range of models. We present the model and a brief review of its inversion to disclose the relationships among, apparently, diverse generative models of empirical data. We then show that this inversion can be formulated as a simple neural network and may provide a useful metaphor for inference and learning in the brain.

          Author Summary

          Models are essential to make sense of scientific data, but they may also play a central role in how we assimilate sensory information. In this paper, we introduce a general model that generates or predicts diverse sorts of data. As such, it subsumes many common models used in data analysis and statistical testing. We show that this model can be fitted to data using a single and generic procedure, which means we can place a large array of data analysis procedures within the same unifying framework. Critically, we then show that the brain has, in principle, the machinery to implement this scheme. This suggests that the brain has the capacity to analyse sensory input using the most sophisticated algorithms currently employed by scientists and possibly models that are even more elaborate. The implications of this work are that we can understand the structure and function of the brain as an inference machine. Furthermore, we can ascribe various aspects of brain anatomy and physiology to specific computational quantities, which may help understand both normal brain function and how aberrant inferences result from pathological processes associated with psychiatric disorders.

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          Most cited references77

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          From sensation to cognition.

          M. Mesulam (1998)
          Sensory information undergoes extensive associative elaboration and attentional modulation as it becomes incorporated into the texture of cognition. This process occurs along a core synaptic hierarchy which includes the primary sensory, upstream unimodal, downstream unimodal, heteromodal, paralimbic and limbic zones of the cerebral cortex. Connections from one zone to another are reciprocal and allow higher synaptic levels to exert a feedback (top-down) influence upon earlier levels of processing. Each cortical area provides a nexus for the convergence of afferents and divergence of efferents. The resultant synaptic organization supports parallel as well as serial processing, and allows each sensory event to initiate multiple cognitive and behavioural outcomes. Upstream sectors of unimodal association areas encode basic features of sensation such as colour, motion, form and pitch. More complex contents of sensory experience such as objects, faces, word-forms, spatial locations and sound sequences become encoded within downstream sectors of unimodal areas by groups of coarsely tuned neurons. The highest synaptic levels of sensory-fugal processing are occupied by heteromodal, paralimbic and limbic cortices, collectively known as transmodal areas. The unique role of these areas is to bind multiple unimodal and other transmodal areas into distributed but integrated multimodal representations. Transmodal areas in the midtemporal cortex, Wernicke's area, the hippocampal-entorhinal complex and the posterior parietal cortex provide critical gateways for transforming perception into recognition, word-forms into meaning, scenes and events into experiences, and spatial locations into targets for exploration. All cognitive processes arise from analogous associative transformations of similar sets of sensory inputs. The differences in the resultant cognitive operation are determined by the anatomical and physiological properties of the transmodal node that acts as the critical gateway for the dominant transformation. Interconnected sets of transmodal nodes provide anatomical and computational epicentres for large-scale neurocognitive networks. In keeping with the principles of selectively distributed processing, each epicentre of a large-scale network displays a relative specialization for a specific behavioural component of its principal neurospychological domain. The destruction of transmodal epicentres causes global impairments such as multimodal anomia, neglect and amnesia, whereas their selective disconnection from relevant unimodal areas elicits modality-specific impairments such as prosopagnosia, pure word blindness and category-specific anomias. The human brain contains at least five anatomically distinct networks. The network for spatial awareness is based on transmodal epicentres in the posterior parietal cortex and the frontal eye fields; the language network on epicentres in Wernicke's and Broca's areas; the explicit memory/emotion network on epicentres in the hippocampal-entorhinal complex and the amygdala; the face-object recognition network on epicentres in the midtemporal and temporopolar cortices; and the working memory-executive function network on epicentres in the lateral prefrontal cortex and perhaps the posterior parietal cortex. Individual sensory modalities give rise to streams of processing directed to transmodal nodes belonging to each of these networks. The fidelity of sensory channels is actively protected through approximately four synaptic levels of sensory-fugal processing. The modality-specific cortices at these four synaptic levels encode the most veridical representations of experience. Attentional, motivational and emotional modulations, including those related to working memory, novelty-seeking and mental imagery, become increasingly more pronounced within downstream components of unimodal areas, where they help to create a highly edited subjective version of the world. (ABSTRACT TRUNCATED)
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            Synaptic plasticity and memory: an evaluation of the hypothesis.

            Changing the strength of connections between neurons is widely assumed to be the mechanism by which memory traces are encoded and stored in the central nervous system. In its most general form, the synaptic plasticity and memory hypothesis states that "activity-dependent synaptic plasticity is induced at appropriate synapses during memory formation and is both necessary and sufficient for the information storage underlying the type of memory mediated by the brain area in which that plasticity is observed." We outline a set of criteria by which this hypothesis can be judged and describe a range of experimental strategies used to investigate it. We review both classical and newly discovered properties of synaptic plasticity and stress the importance of the neural architecture and synaptic learning rules of the network in which it is embedded. The greater part of the article focuses on types of memory mediated by the hippocampus, amygdala, and cortex. We conclude that a wealth of data supports the notion that synaptic plasticity is necessary for learning and memory, but that little data currently supports the notion of sufficiency.
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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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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS Comput Biol
                plos
                ploscomp
                PLoS Computational Biology
                Public Library of Science (San Francisco, USA )
                1553-734X
                1553-7358
                November 2008
                November 2008
                7 November 2008
                : 4
                : 11
                : e1000211
                Affiliations
                [1]The Wellcome Trust Centre of Neuroimaging, University College London, London, United Kingdom
                Indiana University, United States of America
                Author notes

                Conceived and designed the experiments: KJF. Performed the experiments: KJF. Analyzed the data: KJF. Contributed reagents/materials/analysis tools: KJF. Wrote the paper: KJF.

                Article
                08-PLCB-RA-0513R3
                10.1371/journal.pcbi.1000211
                2570625
                18989391
                685f1159-39a4-4fc9-89c6-cb21d2c87d5e
                Karl Friston. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
                History
                : 30 June 2008
                : 19 September 2008
                Page count
                Pages: 24
                Categories
                Research Article
                Mathematics/Statistics
                Neuroscience
                Neuroscience/Theoretical Neuroscience

                Quantitative & Systems biology
                Quantitative & Systems biology

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