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Binocular summation in marmoset lateral geniculate nucleus

Published online by Cambridge University Press:  13 November 2019

Elissa Belluccini ,
Natalie Zeater ,
Alexander N.J. Pietersen ,
Calvin D. Eiber  and
Paul R. Martin Open the ORCID record for Paul R. Martin [Opens in a new window]
Elissa Belluccini
Affiliation:
ARC Centre of Excellence for Integrative Brain Function, University of Sydney, Sydney 2000, Australia Save Sight Institute, University of Sydney, Sydney 2000, Australia School of Medical Sciences, University of Sydney, Sydney 2000, Australia
Natalie Zeater
Affiliation:
ARC Centre of Excellence for Integrative Brain Function, University of Sydney, Sydney 2000, Australia Save Sight Institute, University of Sydney, Sydney 2000, Australia School of Medical Sciences, University of Sydney, Sydney 2000, Australia
Alexander N.J. Pietersen
Affiliation:
ARC Centre of Excellence for Integrative Brain Function, University of Sydney, Sydney 2000, Australia Save Sight Institute, University of Sydney, Sydney 2000, Australia School of Medical Sciences, University of Sydney, Sydney 2000, Australia
Calvin D. Eiber
Affiliation:
ARC Centre of Excellence for Integrative Brain Function, University of Sydney, Sydney 2000, Australia Save Sight Institute, University of Sydney, Sydney 2000, Australia School of Medical Sciences, University of Sydney, Sydney 2000, Australia
Paul R. Martin*
Affiliation:
ARC Centre of Excellence for Integrative Brain Function, University of Sydney, Sydney 2000, Australia Save Sight Institute, University of Sydney, Sydney 2000, Australia School of Medical Sciences, University of Sydney, Sydney 2000, Australia
*
*Address correspondence to: Paul R Martin, Email: [email protected]
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Abstract

In primates and carnivores, the main laminae of the dorsal lateral geniculate nucleus (LGN) receive monocular excitatory input in an eye-alternating fashion. There is also evidence that nondominant eye stimulation can reduce responses to dominant eye stimulation and that a subset of LGN cells in the koniocellular (K) layers receives convergent binocular excitatory input from both eyes. What is not known is how the two eye inputs summate in the K layers of LGN. Here, we aimed to answer this question by making extracellular array electrode recordings targeted to K layers in the marmoset (Callithrix jacchus) LGN, as visual stimuli (flashed 200 ms temporal square-wave pulses or drifting gratings) were presented to each eye independently or to both eyes simultaneously. We found that when the flashed stimulus was presented to both eyes, compared to the dominant eye, the peak firing rate of most cells (61%, 14/23) was reduced. The remainder showed response facilitation (17%) or partial summation (22%). A greater degree of facilitation was seen when the total number of spikes across the stimulus time window (200 ms) rather than peak firing rates was measured. A similar pattern of results was seen for contrast-varying gratings and for small numbers of parvocellular (n = 12) and magnocellular (n = 3) cells recorded. Our findings show that binocular summation in the marmoset LGN is weak and predominantly sublinear in nature.

Keywords

Binocular visionParallel visual pathwaysLateral geniculate nucleusNonhuman primates
Type
Research Article
Information
Visual Neuroscience , Volume 36 , 2019 , E012
Copyright
Copyright © Cambridge University Press 2019 

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References

Bishop, P.O. & Davis, R. (1953). Bilateral interaction in the lateral geniculate body. Science 118, 241–243.CrossRefGoogle ScholarPubMed
Briggs, F. & Usrey, W.M. (2007). A fast, reciprocal pathway between the lateral geniculate nucleus and visual cortex in the macaque monkey. The Journal of Neuroscience 27, 5431–5436.CrossRefGoogle ScholarPubMed
Cheong, S.K., Tailby, C., Martin, P.R., Levitt, J.B. & Solomon, S.G. (2011). Slow intrinsic rhythm in the koniocellular visual pathway. Proceedings of the National Academy of Sciences 108, 14659–14663.CrossRefGoogle ScholarPubMed
Croner, L.J. & Kaplan, E. (1995). Receptive fields of P and M ganglion cells across the primate retina. Vision Research 35, 7–24.CrossRefGoogle Scholar
Dubin, M.W. & Cleland, B.G. (1977). Organization of visual inputs to interneurons of lateral geniculate nucleus of the cat. Journal of Neurophysiology 40, 410–427.CrossRefGoogle ScholarPubMed
Enroth-cugell, C. & Robson, J.G. (1966). The contrast sensitivity of retinal ganglion cells of the cat. The Journal of Physiology 187, 517–552.CrossRefGoogle ScholarPubMed
Glees, P. & Le Gros Clark, W.E. (1941). The termination of optic fibres in the lateral geniculate body of the monkey. Journal of Anatomy 75, 295–308.Google ScholarPubMed
Grieve, K.L. (2005). Binocular visual responses in cells of the rat dLGN. The Journal of Physiology 566, 119–124.CrossRefGoogle ScholarPubMed
Guido, W., Tumosa, N. & Spear, P.D. (1989). Binocular interactions in the cat’s dorsal lateral geniculate nucleus. I. Spatial-frequency analysis of responses of X, Y, and W cells to nondominant-eye stimulation. Journal of Neurophysiology 62, 526–543.CrossRefGoogle Scholar
Guillery, R.W. (1969). A quantitative study of synaptic interconnections in the dorsal lateral geniculate nucleus. Cell and Tissue Research 96, 39–48.Google Scholar
Harting, J.K., Huerta, M.F., Hashikawa, T. & Van Lieshout, D.P. (1991). Projection of the mammalian superior colliculus upon the dorsal lateral geniculate nucleus: Organization of tectogeniculate pathways in nineteen species. The Journal of Comparative Neurology 304, 275–306.CrossRefGoogle ScholarPubMed
Hayhow, W.R. (1958). The cytoarchitecture of the lateral geniculate body in the cat in relation to the distribution of crossed and uncrossed optic fibers. The Journal of Comparative Neurology 110, 1–63.CrossRefGoogle ScholarPubMed
Howarth, M., Walmsley, L. & Brown, T.M. (2014). Binocular integration in the mouse lateral geniculate nuclei. Current Biology 24, 1241–1247.CrossRefGoogle ScholarPubMed
Kaas, J.H., Huerta, M.F., Weber, J.T. & Harting, J.K. (1978). Patterns of retinal terminations and laminar organization of the lateral geniculate nucleus of primates. The Journal of Comparative Neurology 182, 517–553.CrossRefGoogle ScholarPubMed
Kato, H., Bishop, P.O. & Orban, G.A. (1981). Binocular interaction on monocularly discharged lateral geniculate and striate neurons in the cat. Journal of Neurophysiology 46, 932–951.CrossRefGoogle ScholarPubMed
Kaplan, E. (2009) The M, P, and K pathways of the primate visual system revisited. In The New Visual Neurosciences, eds. Werner, J.S. & Chalupa, L.M., pp. 215–226. Cambridge, MA: The MIT Press.Google Scholar
Kwan, W.C., Mundinano, I.C., De Souza, M.J., Lee, S.C.S., Martin, P.R., Grünert, U. & Bourne, J.A. (2018). Unravelling the subcortical and retinal circuitry of the primate inferior pulvinar. The Journal of Comparative Neurology 527, 558–576.CrossRefGoogle ScholarPubMed
Lehky, S.R. & Maunsell, J.H. (1996). No binocular rivalry in the LGN of alert macaque monkeys. Vision Research 36, 1225–1234.CrossRefGoogle ScholarPubMed
Marrocco, R.T. & Mcclurkin, J.W. (1979). Binocular interaction in the lateral geniculate nucleus of the monkey. Brain Research 168, 633–637.CrossRefGoogle ScholarPubMed
Moore, R.J., Spear, P.D., Kim, C.B. & Xue, J.T. (1992). Binocular processing in the cat’s dorsal lateral geniculate nucleus. III. Spatial frequency, orientation, and direction sensitivity of nondominant-eye influences. Experimental Brain Research 89, 588–598.CrossRefGoogle ScholarPubMed
Nassi, J.J. & Callaway, E.M. (2009). Parallel processing strategies of the primate visual system. Nature Reviews Neuroscience 10, 360–372.CrossRefGoogle ScholarPubMed
Pape, H.C. & Eysel, U.T. (1986). Binocular interactions in the lateral geniculate nucleus of the cat: GABAergic inhibition reduced by dominant afferent activity. Experimental Brain Research 61, 265–271.CrossRefGoogle ScholarPubMed
Pollack, J.G. & Hickey, T.L. (1979). The distribution of retino-collicular axon terminals in rhesus monkey. The Journal of Comparative Neurology 185, 587–602.CrossRefGoogle ScholarPubMed
RodiecK, R.W. & Dreher, B. (1979). Visual suppression from nondominant eye in the lateral geniculate nucleus: A comparison of cat and monkey. Experimental Brain Research 35, 465–477.CrossRefGoogle ScholarPubMed
Sanderson, K.J., Bishop, P.O. & Darian-Smith, I. (1971). The properties of the binocular receptive fields of lateral geniculate neurons. Experimental Brain Research 13, 178–207.CrossRefGoogle ScholarPubMed
Sanderson, K.J., Darian-Smith, I. & Bishop, P.O. (1969). Binocular corresponding receptive fields of single units in the cat dorsal lateral geniculate nucleus. Vision Research 9, 1297–1303.CrossRefGoogle ScholarPubMed
Schmielau, F. & Singer, W. (1977). The role of visual cortex for binocular interactions in the cat lateral geniculate nucleus. Brain Research 120, 354–361.CrossRefGoogle ScholarPubMed
Schroeder, C.E., Tenke, C.E., Arezzo, J.C. & Vaughan, H.G. (1990). Binocularity in the lateral geniculate nucleus of the alert macaque. Brain Research 521, 303–310.CrossRefGoogle ScholarPubMed
Sengpiel, F., Blakemore, C. & Harrad, R. (1995). Interocular suppression in the primary visual cortex: A possible neural basis of binocular rivalry. Vision Research 35, 179–195.CrossRefGoogle ScholarPubMed
Singer, W. (1970). Inhibitory binocular interaction in the lateral geniculate body of the cat. Brain Research 18, 165–170.CrossRefGoogle ScholarPubMed
Sivyer, B., Taylor, W.R. & Vaney, D.I. (2010). Uniformity detector retinal ganglion cells fire complex spikes and receive only light-evoked inhibition. Proceedings of the National Academy of Sciences 107, 5628–5633.CrossRefGoogle ScholarPubMed
Solomon, S.G., White, A.J.R. & Martin, P.R. (2002). Extraclassical receptive field properties of parvocellular, magnocellular and koniocellular cells in the primate lateral geniculate nucleus. Journal of Neuroscience 22, 338–349.CrossRefGoogle ScholarPubMed
Solomon, S.G., Tailby, C., Cheong, S.K. & Camp, A.J. (2010). Linear and non-linear contributions to the visual sensitivity of neurons in primate lateral geniculate nucleus. Journal of Neurophysiology 104, 1884–1898.CrossRefGoogle Scholar
Suzuki, H. & Kato, E. (1966). Binocular interaction at cat’s lateral geniculate body. Journal of Neurophysiology 29, 909–920.CrossRefGoogle ScholarPubMed
Tailby, C., Szmajda, B.A., Buzás, P., Lee, B.B. & Martin, P.R. (2008). Transmission of blue (S) cone signals through the primate lateral geniculate nucleus. The Journal of Physiology 586, 5947–5967.CrossRefGoogle ScholarPubMed
Tong, L., Guido, W., Tumosa, N., Spear, P.D. & Heidenreich, S. (1992). Binocular interactions in the cat’s dorsal lateral geniculate nucleus, II: Effects on dominant-eye spatial-frequency and contrast processing. Visual Neuroscience 8, 557–566.CrossRefGoogle ScholarPubMed
Xue, J.T., Ramoa, A.S., Carney, T. & Freeman, R.D. (1987). Binocular interaction in the dorsal lateral geniculate nucleus of the cat. Experimental Brain Research 68, 305–310.CrossRefGoogle ScholarPubMed
Zeater, N., Buzás, P., Dreher, B., grünert, U. & Martin, P.R. (2019). Projections of three subcortical visual centers to marmoset lateral geniculate nucleus. The Journal of Comparative Neurology 527, 535–545.CrossRefGoogle ScholarPubMed
Zeater, N., Cheong, S.K., Solomon, S.G., Dreher, B. & Martin, P.R. (2015). Binocular visual responses in the primate lateral geniculate nucleus. Current Biology 25, 3190–3195.CrossRefGoogle ScholarPubMed