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      Canonical Cortical Circuit Model Explains Rivalry, Intermittent Rivalry, and Rivalry Memory

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          Abstract

          It has been shown that the same canonical cortical circuit model with mutual inhibition and a fatigue process can explain perceptual rivalry and other neurophysiological responses to a range of static stimuli. However, it has been proposed that this model cannot explain responses to dynamic inputs such as found in intermittent rivalry and rivalry memory, where maintenance of a percept when the stimulus is absent is required. This challenges the universality of the basic canonical cortical circuit. Here, we show that by including an overlooked realistic small nonspecific background neural activity, the same basic model can reproduce intermittent rivalry and rivalry memory without compromising static rivalry and other cortical phenomena. The background activity induces a mutual-inhibition mechanism for short-term memory, which is robust to noise and where fine-tuning of recurrent excitation or inclusion of sub-threshold currents or synaptic facilitation is unnecessary. We prove existence conditions for the mechanism and show that it can explain experimental results from the quartet apparent motion illusion, which is a prototypical intermittent rivalry stimulus.

          Author Summary

          When the brain is presented with an ambiguous stimulus like the Necker cube or what is known as the quartet illusion, the perception will alternate or rival between the possible interpretations. There are neurons in the brain whose activity is correlated with the perception and not the stimulus. Hence, perceptual rivalry provides a unique probe of cortical function and could possibly serve as a diagnostic tool for cognitive disorders such as autism. A mathematical model based on the known biology of the brain has been developed to account for perceptual rivalry when the stimulus is static. The basic model also accounts for other neural responses to stimuli that do not elicit rivalry. However, these models cannot explain illusions where the stimulus is intermittently switched on and off and the same perception returns after an off period because there is no built-in mechanism to hold the memory. Here, we show that the inclusion of experimentally observed low-level background neural activity is sufficient to explain rivalry for static inputs, and rivalry for intermittent inputs. We validate the model with new experiments.

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          Most cited references33

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          Normalization as a canonical neural computation.

          There is increasing evidence that the brain relies on a set of canonical neural computations, repeating them across brain regions and modalities to apply similar operations to different problems. A promising candidate for such a computation is normalization, in which the responses of neurons are divided by a common factor that typically includes the summed activity of a pool of neurons. Normalization was developed to explain responses in the primary visual cortex and is now thought to operate throughout the visual system, and in many other sensory modalities and brain regions. Normalization may underlie operations such as the representation of odours, the modulatory effects of visual attention, the encoding of value and the integration of multisensory information. Its presence in such a diversity of neural systems in multiple species, from invertebrates to mammals, suggests that it serves as a canonical neural computation.
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            Dynamics of pattern formation in lateral-inhibition type neural fields.

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              Synaptic mechanisms and network dynamics underlying spatial working memory in a cortical network model.

              Single-neuron recordings from behaving primates have established a link between working memory processes and information-specific neuronal persistent activity in the prefrontal cortex. Using a network model endowed with a columnar architecture and based on the physiological properties of cortical neurons and synapses, we have examined the synaptic mechanisms of selective persistent activity underlying spatial working memory in the prefrontal cortex. Our model reproduces the phenomenology of the oculomotor delayed-response experiment of Funahashi et al. (S. Funahashi, C.J. Bruce and P.S. Goldman-Rakic, Mnemonic coding of visual space in the monkey's dorsolateral prefrontal cortex. J Neurophysiol 61:331-349, 1989). To observe stable spontaneous and persistent activity, we find that recurrent synaptic excitation should be primarily mediated by NMDA receptors, and that overall recurrent synaptic interactions should be dominated by inhibition. Isodirectional tuning of adjacent pyramidal cells and interneurons can be accounted for by a structured pyramid-to-interneuron connectivity. Robust memory storage against random drift of the tuned persistent activity and against distractors (intervening stimuli during the delay period) may be enhanced by neuromodulation of recurrent synapses. Experimentally testable predictions concerning the neural basis of working memory are discussed.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS Comput Biol
                PLoS Comput. Biol
                plos
                ploscomp
                PLoS Computational Biology
                Public Library of Science (San Francisco, CA USA )
                1553-734X
                1553-7358
                3 May 2016
                May 2016
                : 12
                : 5
                : e1004903
                Affiliations
                [1 ]Mathematical Biology Section, Laboratory of Biological Modeling, National Institutes of Diabetes and Digestive and Kidney Disease, National Institutes of Health, Bethesda, Maryland, United States of America
                [2 ]Cognitive Neuropsychology Section, Laboratory of Brain and Cognition, National Institute of Mental Health, National Institutes of Health, Bethesda, Maryland, United States of America
                University College London, UNITED KINGDOM
                Author notes

                The authors have declared that no competing interests exist.

                Conceived and designed the experiments: SV CCC SJG AM. Performed the experiments: SV CCC PT HWX. Analyzed the data: SV CCC. Wrote the paper: SV CCC SJG AM PT.

                Author information
                http://orcid.org/0000-0003-3968-1563
                Article
                PCOMPBIOL-D-15-01402
                10.1371/journal.pcbi.1004903
                4854419
                27138214
                cbd98368-6fa3-4435-af60-50e516ec0007

                This is an open access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.

                History
                : 26 August 2015
                : 6 April 2016
                Page count
                Figures: 11, Tables: 0, Pages: 22
                Funding
                This work was supported by the Intramural Research Program of the NIH, NIDDK and NIMH. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
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