The influence of surround suppression on adaptation effects in primary visual cortex

Wissig, Stephanie; Kohn, Adam

doi:10.1152/jn.00739.2011

Cited by 106 publications

(163 citation statements)

References 83 publications

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“…Subsets of cells responding to repeated visual stimulation with sensitization have been described in the retina (Kastner and Baccus 2011), LGN (Camp et al 2009), and cortex (Wissig and Kohn 2012). Psychophysical experiments have demonstrated enhanced sensitivity following stimulus deprivation (Zhang et al 2009), which may be related to the increased spontaneous rate that we found after prolonged neuronal response suppression.…”

Section: Discussionsupporting

confidence: 65%

Hour-long adaptation in the awake early visual system

Stoelzel

Huff

Bereshpolova

et al. 2015

Journal of Neurophysiology

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Sensory adaptation serves to adjust awake brains to changing environments on different time scales. However, adaptation has been studied traditionally under anesthesia and for short time periods. Here, we demonstrate in awake rabbits a novel type of sensory adaptation that persists for Ͼ1 h and acts on visual thalamocortical neurons and their synapses in the input layers of the visual cortex. Following prolonged visual stimulation (10 -30 min), cells in the dorsal lateral geniculate nucleus (LGN) show a severe and prolonged reduction in spontaneous firing rate. This effect is bidirectional, and prolonged visually induced response suppression is followed by a prolonged increase in spontaneous activity. The reduction in thalamic spontaneous activity following prolonged visual activation is accompanied by increases in 1) response reliability, 2) signal detectability, and 3) the ratio of visual signal/spontaneous activity. In addition, following such prolonged activation of an LGN neuron, the monosynaptic currents generated by thalamic impulses in layer 4 of the primary visual cortex are enhanced. These results demonstrate that in awake brains, prolonged sensory stimulation can have a profound, long-lasting effect on the information conveyed by thalamocortical inputs to the visual cortex. lateral geniculate nucleus; thalamocortical; sensory adaptation THE VISUAL SYSTEM IS HIGHLY dynamic, able to scale neuronal responses across several orders of magnitude of mean luminance and to alter tuning specificity based on recent visual experience. Adaptations of neural responses, lasting from seconds (Baccus and Meister 2002;Brown and Masland 2001;Rieke 2001) to minutes (Dragoi et al. 2000;Giaschi et al. 1993;Hammond et al. 1988;McLelland et al. 2009;Ohzawa et al. 1985;Vautin and Berkley 1977), have been described, with the longest lasting adaption ϳ10 min (Dragoi et al. 2000). Yet, the perceptual effects of long-duration adapting stimuli can last considerably longer [see, for example, Dong et al. (2014) Here, we describe a novel form of adaptation, following prolonged visual stimulation, in which the spontaneous activity of neurons in the lateral geniculate nucleus (LGN) of awake rabbits is reduced to as little as 10% of pre-adaptation baseline activity levels and slowly recovers over a period of Ͼ1 h. We demonstrate that this adaptation, which is cell specific and retinotopically precise, is accompanied by an increase in the reliability (reduced Fano factor) and detectability [increased area of receiver operator characteristic (ROC) functions] of visual responses and by an increase in the ratio of evoked-tospontaneous firing rates. We also show that during the adapted period, monosynaptic currents, generated in layer 4 by thalamic impulses, are greatly increased, providing a mechanism for further enhancing the saliency of visual stimuli. Finally, we show that visual stimuli that suppress cell responses for a prolonged period of time can have the opposite effect and generate a prolonged increase in thalamic spontaneous activ...

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Section: Discussionsupporting

confidence: 65%

Hour-long adaptation in the awake early visual system

Stoelzel

Huff

Bereshpolova

et al. 2015

Journal of Neurophysiology

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“…Attentional modulation also involves normalization (Reynolds and Heeger, 2009;Sundberg et al, 2009;Lee and Maunsell, 2010;Ni et al, 2012;Schwartz and Coen-Cagli, 2013) and it too weakens correlations (Cohen and Maunsell, 2009;Mitchell et al, 2009). Finally, adaptation may affect normalization signals (Wainwright et al, 2002;Wissig and Kohn, 2012), and it also alters correlations (Gutnisky and Dragoi, 2008;Adibi et al, 2013). Note that although these many different forms of modulation have been cast as involving normalization, they may involve distinct cellular and circuit processes.…”

Section: Discussionmentioning

confidence: 99%

Correlations in V1 Are Reduced by Stimulation Outside the Receptive Field

et al. 2014

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The trial-to-trial response variability of nearby cortical neurons is correlated. These correlations may strongly influence population coding performance. Numerous studies have shown that correlations can be dynamically modified by attention, adaptation, learning, and potent stimulus drive. However, the mechanisms that influence correlation strength remain poorly understood. Here we test whether correlations are influenced by presenting stimuli outside the classical receptive field (RF) of visual neurons, where they recruit a normalization signal termed surround suppression. We recorded simultaneously the activity of dozens of cells using microelectrode arrays implanted in the superficial layers of V1 in anesthetized, paralyzed macaque monkeys. We presented annular stimuli that encircled-but did not impinge upon-the RFs of the recorded cells. We found that these "extra-classical" stimuli reduced correlations in the absence of stimulation of the RF, closely resembling the decorrelating effects of stimulating the RFs directly. Our results suggest that normalization signals may be an important mechanism for modulating correlations.

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“…It has been suggested that the weights of divisive normalization are optimized to improve the efficiency of sensory coding Wainwright et al, 2002;Sinz and Bethge, 2013). Divisive normalization (or gain control) has also been used to explain some adaptation phenomena (Ohzawa et al, 1982;Heeger, 1992b;Wainwright et al, 2002;Wissig and Kohn, 2012;Solomon and Kohn, 2014). The model that we propose updates the normalization weights between each pair of neurons based on the product of their responses and could be implemented by a simple synaptic mechanism for coincidence detection (Levy and Steward, 1983;Yao and Dan, 2001;Yao et al, 2004).…”

Section: Introductionmentioning

confidence: 99%

Pattern Adaptation and Normalization Reweighting

Westrick¹,

Heeger

Landy

2016

J. Neurosci.

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Adaptation to an oriented stimulus changes both the gain and preferred orientation of neural responses in V1. Neurons tuned near the adapted orientation are suppressed, and their preferred orientations shift away from the adapter. We propose a model in which weights of divisive normalization are dynamically adjusted to homeostatically maintain response products between pairs of neurons. We demonstrate that this adjustment can be performed by a very simple learning rule. Simulations of this model closely match existing data from visual adaptation experiments. We consider several alternative models, including variants based on homeostatic maintenance of response correlations or covariance, as well as feedforward gain-control models with multiple layers, and we demonstrate that homeostatic maintenance of response products provides the best account of the physiological data.

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The influence of surround suppression on adaptation effects in primary visual cortex

Cited by 106 publications

References 83 publications

Hour-long adaptation in the awake early visual system

Hour-long adaptation in the awake early visual system

Correlations in V1 Are Reduced by Stimulation Outside the Receptive Field

Pattern Adaptation and Normalization Reweighting

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