Generation of Black-Dominant Responses in V1 Cortex

Xing, Dajun; Yeh, Chun-I; Shapley, Robert

doi:10.1523/jneurosci.2473-10.2010

Cited by 85 publications

(100 citation statements)

References 47 publications

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“…Surprisingly, although most textbooks assume that ON and OFF visual responses are balanced throughout the visual system, recent studies have identified a pronounced overrepresentation of the OFF visual responses in primary visual cortex (area V1) (1)(2)(3). This recent discovery resonates with pioneering studies by Galilei (4) and von Helmholtz (5) who noticed that visual spatial resolution was higher for dark than light stimuli.…”

mentioning

confidence: 68%

Neuronal nonlinearity explains greater visual spatial resolution for darks than lights

Kremkow

Jin

Komban

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

132

229

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Astronomers and physicists noticed centuries ago that visual spatial resolution is higher for dark than light stimuli, but the neuronal mechanisms for this perceptual asymmetry remain unknown. Here we demonstrate that the asymmetry is caused by a neuronal nonlinearity in the early visual pathway. We show that neurons driven by darks (OFF neurons) increase their responses roughly linearly with luminance decrements, independent of the background luminance. However, neurons driven by lights (ON neurons) saturate their responses with small increases in luminance and need bright backgrounds to approach the linearity of OFF neurons. We show that, as a consequence of this difference in linearity, receptive fields are larger in ON than OFF thalamic neurons, and cortical neurons are more strongly driven by darks than lights at low spatial frequencies. This ON/OFF asymmetry in linearity could be demonstrated in the visual cortex of cats, monkeys, and humans and in the cat visual thalamus. Furthermore, in the cat visual thalamus, we show that the neuronal nonlinearity is present at the ON receptive field center of ONcenter neurons and ON receptive field surround of OFF-center neurons, suggesting an origin at the level of the photoreceptor. These results demonstrate a fundamental difference in visual processing between ON and OFF channels and reveal a competitive advantage for OFF neurons over ON neurons at low spatial frequencies, which could be important during cortical development when retinal images are blurred by immature optics in infant eyes.neuronal coding | lateral geniculate nucleus | area V1 | irradiation illusion | LFP L ight and dark stimuli are separately processed by ON and OFF channels in the retina and visual thalamus. Surprisingly, although most textbooks assume that ON and OFF visual responses are balanced throughout the visual system, recent studies have identified a pronounced overrepresentation of the OFF visual responses in primary visual cortex (area V1) (1-3). This recent discovery resonates with pioneering studies by Galilei (4) and von Helmholtz (5) who noticed that visual spatial resolution was higher for dark than light stimuli. Galilei (4) related the difference in resolution to the observation that a light patch on a dark background appears larger than the same sized dark patch on a light background, an illusion that von Helmholtz (5) named the "irradiation illusion." Although this illusion has been studied in the past (6, 7), its underlying neuronal mechanisms remain unknown. It has been suggested that the perceived size differences could be caused by the light scatter in the optics of the eye followed by a neuronal nonlinearity (6, 7), but there are no neuronal measurements of a nonlinearity that fits the explanation. Previous studies revealed differences in response linearity between ON and OFF retinal ganglion cells (8, 9) and horizontal cells (10). However, a main conclusion from these studies was that ON retinal ganglion cells were roughly linear and less rectified than OFF retinal gangl...

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mentioning

confidence: 68%

Neuronal nonlinearity explains greater visual spatial resolution for darks than lights

Kremkow

Jin

Komban

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

132

229

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“…For example, OFF neurons may be less effective (i.e., being weighted less) than ON neurons in driving downstream V1 neurons. Considering the fact that OFF neuron projections dominate the cortical representation of central vision (Jin et al 2008(Jin et al , 2011, and that visual responses to dark stimuli dominate the superficial layers of V1 (Xing et al 2010;Yeh et al 2009), this explanation is unlikely to be true, but it cannot be completely dismissed either. Another possibility is that LGN M OFF neurons, which we did not analyze in this study, may contribute more to decrement detection than P OFF neurons.…”

Section: Choice-related Activitymentioning

confidence: 99%

“…More specifically, do darks have access to more neuronal resources than lights in the early visual pathway (Ahmad et al 2003;Jin et al 2008;Pandarinath et al 2010;Ratliff et al 2010;Xing et al 2010;Yeh et al 2009)? If so, is this difference sufficient to explain why psychophysically darks appear more salient and are detected faster than lights?…”

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confidence: 99%

The functional asymmetry of ON and OFF channels in the perception of contrast

Jiang

Purushothaman

Casagrande

2015

Journal of Neurophysiology

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-To fully understand the relationship between perception and single neural responses, one should take into consideration the early stages of sensory processing. Few studies, however, have directly examined the neural underpinning of visual perception in the lateral geniculate nucleus (LGN), only one synapse away from the retina. In this study we recorded from LGN parvocellular (P) ON-center and OFF-center neurons while monkeys either passively viewed or actively detected a full range of contrasts. We found that OFF neurons were more sensitive in detecting negative contrasts than ON neurons were in detecting positive contrasts. Also, OFF neurons had higher spontaneous activities, higher peak response amplitudes, and were more sustained than ON neurons in their contrast responses. Puzzlingly, OFF neurons failed to show any significant correlations with the monkeys' perceptual choices, despite their greater contrast sensitivities. If, however, choice probabilities were calculated from interspike intervals instead of spike counts (thus taking into account the higher firing rates of OFF neurons), OFF neurons but not ON neurons were significantly correlated with behavioral choices. Taken together, these results demonstrate in awake, behaving animals that: 1) the ON and OFF pathways do not simply mirror each other in their functionality but instead carry qualitatively different types of information, and 2) the responses of ON and OFF neurons can be correlated with perceptual choices even in the absence of physical stimuli and interneuronal correlations. lateral geniculate nucleus; ON-center cell; OFF-center cell; contrast detection; choice probability EARLY PSYCHOPHYSICAL STUDIES indicated that separate channels underlie our perception of brightness (i.e., positive contrasts, or luminance increments) and darkness (i.e., negative contrasts, or luminance decrements), respectively

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“…Extrastriate cortical feedback targets layers 2, 3, and 6 (1,3,7). The visual functional properties of cells in different layers are markedly different (2,(8)(9)(10)(11)(12)(13), reflecting local circuitry that is layer-specific (1,3,6). Because of the similarities of laminar cortical circuitry throughout the cerebral cortex (14-16), we used V1 as a test bed to study laminar patterns of stimulus-driven responses.…”

mentioning

confidence: 99%

Laminar analysis of visually evoked activity in the primary visual cortex

Xing

Yeh

Burns

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

189

166

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Studying the laminar pattern of neural activity is crucial for understanding the processing of neural signals in the cerebral cortex. We measured neural population activity [multiunit spike activity (MUA) and local field potential, LFP] in Macaque primary visual cortex (V1) in response to drifting grating stimuli. Sustained visually driven MUA was at an approximately constant level across cortical depth in V1. However, sustained, visually driven, local field potential power, which was concentrated in the γ-band (20-60 Hz), was greatest at the cortical depth corresponding to corticocortical output layers 2, 3, and 4B. γ-band power also tends to be more sustained in the output layers. Overall, cortico-cortical output layers accounted for 67% of total γ-band activity in V1, whereas 56% of total spikes evoked by drifting gratings were from layers 2, 3, and 4B. The high-resolution layer specificity of γ-band power, the laminar distribution of MUA and γ-band activity, and their dynamics imply that neural activity in V1 is generated by laminar-specific mechanisms. In particular, visual responses of MUA and γ-band activity in cortico-cortical output layers 2, 3, and 4B seem to be strongly influenced by laminar-specific recurrent circuitry and/or feedback.B ased on anatomy and neurophysiology, our view of the cerebral cortex has changed. Instead of viewing the cortex as a single network, we now conceive of the cortical laminae as a stack of loosely interconnected but distinct neuronal networks (1-5). Each lamina has different specific inputs, projection targets, and feedback connections.The goal of this study is the determination of the spatial distribution of stimulus-driven neural activity throughout the depth of the cortex and across cortical laminae. Pursuing this goal, we chose to study Macaque primary visual cortex (V1), because V1 is a cortical area where the experimenter has control of the neuronal input by controlling visual stimulation. V1 laminar inputs, outputs, and local connections are well-known (1, 3, 6). Signals come from the thalamus [lateral geniculate nucleus (LGN)] into V1 layers 4C and 6. After intracortical processing, neuronal signals are routed to other cortical areas from cells in superficial layers 2, 3, and 4B of V1; subcortical targets receive cortical outputs from cells in layers 5 and 6. Extrastriate cortical feedback targets layers 2, 3, and 6 (1, 3, 7). The visual functional properties of cells in different layers are markedly different (2, 8-13), reflecting local circuitry that is layer-specific (1, 3, 6). Because of the similarities of laminar cortical circuitry throughout the cerebral cortex (14-16), we used V1 as a test bed to study laminar patterns of stimulus-driven responses.To sample from many neurons in each layer, we measured multiunit spike activity (MUA) and the local field potential (LFP) with multiple microelectrodes (Methods details the operational definitions of MUA and LFP). We measured the power in the LFP at frequencies < 100 Hz, because the largest changes in LFP power...

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Generation of Black-Dominant Responses in V1 Cortex

Cited by 85 publications

References 47 publications

Neuronal nonlinearity explains greater visual spatial resolution for darks than lights

Neuronal nonlinearity explains greater visual spatial resolution for darks than lights

The functional asymmetry of ON and OFF channels in the perception of contrast

Laminar analysis of visually evoked activity in the primary visual cortex

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