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      Flexible Gating of Contextual Influences in Natural Vision

      research-article
      1 , 1 , 2 , 3 , 1 , 3
      Nature neuroscience

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          Abstract

          Identical sensory inputs can be perceived as strikingly different when embedded in distinct contexts. Neural responses to simple stimuli are also modulated by context, but the contribution of this modulation to the processing of natural sensory input is unclear. We measured surround suppression, a quintessential contextual influence, in macaque primary visual cortex with natural images. We found suppression strength varied substantially for different images. This variability was not well explained by existing descriptions of surround suppression, but it was predicted by Bayesian inference about statistical dependencies in images. In this framework, surround suppression was flexible: it was recruited when the image was inferred to contain redundancies, and substantially reduced in strength otherwise. Our results thus reveal a surprising gating of a basic, widespread cortical computation, by inference about the statistics of natural input.

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          Most cited references48

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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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            Cortical interneurons that specialize in disinhibitory control

            In the mammalian cerebral cortex, the diversity of interneuronal subtypes underlies a division of labor subserving distinct modes of inhibitory control 1–7 . A unique mode of inhibitory control may be provided by inhibitory neurons that specifically suppress the firing of other inhibitory neurons. Such disinhibition could lead to the selective amplification of local processing and serve the important computational functions of gating and gain modulation 8,9 . Although several interneuron populations are known to target other interneurons to varying degrees 10–15 , little is known about interneurons specializing in disinhibition and their in vivo function. Here we show that a class of interneurons that express vasoactive intestinal polypeptide (VIP) mediates disinhibitory control in multiple areas of neocortex and is recruited by reinforcement signals. By combining optogenetic activation with single cell recordings, we examined the functional role of VIP interneurons in awake mice, and investigated the underlying circuit mechanisms in vitro in auditory and medial prefrontal cortices. We identified a basic disinhibitory circuit module in which activation of VIP interneurons transiently suppresses primarily somatostatin- and a fraction of parvalbumin-expressing inhibitory interneurons that specialize in the control of the input and output of principal cells, respectively 3,6,16,17 . During the performance of an auditory discrimination task, reinforcement signals (reward and punishment) strongly and uniformly activated VIP neurons in auditory cortex, and in turn VIP recruitment increased the gain of a functional subpopulation of principal neurons. These results reveal a specific cell-type and microcircuit underlying disinhibitory control in cortex and demonstrate that it is activated under specific behavioural conditions.
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              Normalization of cell responses in cat striate cortex.

              D. Heeger (1992)
              Simple cells in the striate cortex have been depicted as half-wave-rectified linear operators. Complex cells have been depicted as energy mechanisms, constructed from the squared sum of the outputs of quadrature pairs of linear operators. However, the linear/energy model falls short of a complete explanation of striate cell responses. In this paper, a modified version of the linear/energy model is presented in which striate cells mutually inhibit one another, effectively normalizing their responses with respect to stimulus contrast. This paper reviews experimental measurements of striate cell responses, and shows that the new model explains a significantly larger body of physiological data.
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                Author and article information

                Journal
                9809671
                21092
                Nat Neurosci
                Nat. Neurosci.
                Nature neuroscience
                1097-6256
                1546-1726
                16 September 2015
                05 October 2015
                November 2015
                01 May 2016
                : 18
                : 11
                : 1648-1655
                Affiliations
                [1 ]D.P. Purpura Department of Neuroscience, Albert Einstein College of Medicine
                [2 ]Department of Ophthalmology and Visual Sciences, Albert Einstein College of Medicine
                [3 ]Department of Systems and Computational Biology, Albert Einstein College of Medicine
                Author notes
                Correspondence should be addressed to R.C.C. ( ruben.coencagli@ 123456gmail.com )
                [4]

                Current address: Department of Computer Science, University of Miami.

                [†]

                Current address: Department of Basic Neuroscience, University of Geneva.

                [*]

                Equal contribution.

                Article
                NIHMS721927
                10.1038/nn.4128
                4624479
                26436902
                9bf7a7c6-8303-4c47-8c70-04148abf365f

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                Neurosciences
                Neurosciences

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