Cortical Balance Between ON and OFF Visual Responses Is Modulated by the Spatial Properties of the Visual Stimulus

Overview

Journal Cereb Cortex

Publisher Oxford University Press

Specialty Neurology

Date 2018 Oct 16

PMID 30321290

Citations 27

Authors

Michael Jansen

Jianzhong Jin

Xiaobing Li

Reza Lashgari

Jens Kremkow

Yulia Bereshpolova

Harvey A Swadlow

Qasim Zaidi

Jose-Manuel Alonso

Affiliations

Soon will be listed here.

Abstract

The primary visual cortex of carnivores and primates is dominated by the OFF visual pathway and responds more strongly to dark than light stimuli. Here, we demonstrate that this cortical OFF dominance is modulated by the size and spatial frequency of the stimulus in awake primates and we uncover a main neuronal mechanism underlying this modulation. We show that large grating patterns with low spatial frequencies drive five times more OFF-dominated than ON-dominated neurons, but this pronounced cortical OFF dominance is strongly reduced when the grating size decreases and the spatial frequency increases, as when the stimulus moves away from the observer. We demonstrate that the reduction in cortical OFF dominance is not caused by a selective reduction of visual responses in OFF-dominated neurons but by a change in the ON/OFF response balance of neurons with diverse receptive field properties that can be ON or OFF dominated, simple, or complex. We conclude that cortical OFF dominance is continuously adjusted by a neuronal mechanism that modulates ON/OFF response balance in multiple cortical neurons when the spatial properties of the visual stimulus change with viewing distance and/or optical blur.

Citing Articles

Retinal Responses to Short- and Longer-Term Predominant ON or OFF Stimulation in Emmetropes and Myopes.

Wagner S, Settele A, Strasser T Invest Ophthalmol Vis Sci. 2025; 66(2):66.

PMID: 40009370 PMC: 11875035. DOI: 10.1167/iovs.66.2.66.

Effects of computer-generated patterns with different temporal and spatial frequencies on choroidal thickness, retinal dopamine and candidate genes in chickens wearing lenses.

Liu H, Schaeffel F, Feldkaemper M Front Med (Lausanne). 2024; 11:1469275.

PMID: 39720655 PMC: 11666368. DOI: 10.3389/fmed.2024.1469275.

Visual Field Asymmetries in Responses to ON and OFF Pathway Biasing Stimuli.

Scott M, Yakovleva A, Norcia A Vis Neurosci. 2024; 41():E007.

PMID: 39698978 PMC: 11730990. DOI: 10.1017/S095252382400004X.

Good vision without peripheries: behavioral and fMRI evidence.

Ninghetto M, Kozak A, Galecki T, Szulborski K, Szaflik J, Oldak M Sci Rep. 2024; 14(1):26264.

PMID: 39487160 PMC: 11530436. DOI: 10.1038/s41598-024-76879-9.

OPTICAL BLUR AFFECTS DIFFERENTLY ON AND OFF VISUAL PATHWAYS.

Pons C, Mazade R, Jin J, Dul M, Alonso J bioRxiv. 2024; .

PMID: 39484435 PMC: 11526864. DOI: 10.1101/2024.10.17.618707.

References

Buchner A, Baumgartner N . Text - background polarity affects performance irrespective of ambient illumination and colour contrast. Ergonomics. 2007; 50(7):1036-63. DOI: 10.1080/00140130701306413. View

Fournier J, Monier C, Levy M, Marre O, Sari K, Kisvarday Z . Hidden complexity of synaptic receptive fields in cat V1. J Neurosci. 2014; 34(16):5515-28. PMC: 6608221. DOI: 10.1523/JNEUROSCI.0474-13.2014. View

Motoyoshi I, Nishida S, Sharan L, Adelson E . Image statistics and the perception of surface qualities. Nature. 2007; 447(7141):206-9. DOI: 10.1038/nature05724. View

Xing D, Shapley R, Hawken M, Ringach D . Effect of stimulus size on the dynamics of orientation selectivity in Macaque V1. J Neurophysiol. 2005; 94(1):799-812. DOI: 10.1152/jn.01139.2004. View

Zaghloul K, Boahen K, Demb J . Different circuits for ON and OFF retinal ganglion cells cause different contrast sensitivities. J Neurosci. 2003; 23(7):2645-54. PMC: 6742092. View

Wassle H, BOYCOTT B, ILLING R . Morphology and mosaic of on- and off-beta cells in the cat retina and some functional considerations. Proc R Soc Lond B Biol Sci. 1981; 212(1187):177-95. DOI: 10.1098/rspb.1981.0033. View

Chen Y, Martinez-Conde S, Macknik S, Bereshpolova Y, Swadlow H, Alonso J . Task difficulty modulates the activity of specific neuronal populations in primary visual cortex. Nat Neurosci. 2008; 11(8):974-82. PMC: 2553692. DOI: 10.1038/nn.2147. View

Veit J, Bhattacharyya A, Kretz R, Rainer G . On the relation between receptive field structure and stimulus selectivity in the tree shrew primary visual cortex. Cereb Cortex. 2013; 24(10):2761-71. DOI: 10.1093/cercor/bht133. View

Schwartz O, Pillow J, Rust N, Simoncelli E . Spike-triggered neural characterization. J Vis. 2006; 6(4):484-507. DOI: 10.1167/6.4.13. View

10.

Smith G, Whitney D, Fitzpatrick D . Modular Representation of Luminance Polarity in the Superficial Layers of Primary Visual Cortex. Neuron. 2015; 88(4):805-18. PMC: 4753785. DOI: 10.1016/j.neuron.2015.10.019. View

11.

Zemon V, Gordon J, Welch J . Asymmetries in ON and OFF visual pathways of humans revealed using contrast-evoked cortical potentials. Vis Neurosci. 1988; 1(1):145-50. DOI: 10.1017/s0952523800001085. View

12.

Ringach D, Shapley R, Hawken M . Orientation selectivity in macaque V1: diversity and laminar dependence. J Neurosci. 2002; 22(13):5639-51. PMC: 6758222. DOI: 20026567. View

13.

Adelson E, Bergen J . Spatiotemporal energy models for the perception of motion. J Opt Soc Am A. 1985; 2(2):284-99. DOI: 10.1364/josaa.2.000284. View

14.

Kontsevich L, Tyler C . Nonlinearities of near-threshold contrast transduction. Vision Res. 1999; 39(10):1869-80. DOI: 10.1016/s0042-6989(98)00286-7. View

15.

Derrington A, Krauskopf J, Lennie P . Chromatic mechanisms in lateral geniculate nucleus of macaque. J Physiol. 1984; 357:241-65. PMC: 1193257. DOI: 10.1113/jphysiol.1984.sp015499. View

16.

DeAngelis G, Ohzawa I, Freeman R . Spatiotemporal organization of simple-cell receptive fields in the cat's striate cortex. I. General characteristics and postnatal development. J Neurophysiol. 1993; 69(4):1091-117. DOI: 10.1152/jn.1993.69.4.1091. View

17.

Samonds J, Potetz B, Lee T . Relative luminance and binocular disparity preferences are correlated in macaque primary visual cortex, matching natural scene statistics. Proc Natl Acad Sci U S A. 2012; 109(16):6313-8. PMC: 3341027. DOI: 10.1073/pnas.1200125109. View

18.

Jin J, Weng C, Yeh C, Gordon J, Ruthazer E, Stryker M . On and off domains of geniculate afferents in cat primary visual cortex. Nat Neurosci. 2007; 11(1):88-94. PMC: 2556869. DOI: 10.1038/nn2029. View

19.

Swindale N, Grinvald A, Shmuel A . The spatial pattern of response magnitude and selectivity for orientation and direction in cat visual cortex. Cereb Cortex. 2003; 13(3):225-38. DOI: 10.1093/cercor/13.3.225. View

20.

Touryan J, Felsen G, Dan Y . Spatial structure of complex cell receptive fields measured with natural images. Neuron. 2005; 45(5):781-91. DOI: 10.1016/j.neuron.2005.01.029. View