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Bypassing V1: a direct geniculate input to area MT

Nature Neuroscience volume 7, pages 1123–1128 (2004)Cite this article

Abstract

Thalamic nuclei are thought to funnel sensory information to the brain's primary cortical areas, which in turn transmit signals afresh to higher cortical areas. Here we describe a direct projection in the macaque monkey from the lateral geniculate nucleus (LGN) to the motion-selective middle temporal area (MTor V5), a cortical area not previously considered 'primary'. The constituent neurons are mostly koniocellular, send virtually no collateral axons to primary visual cortex (V1) and equal about 10% of the V1 population innervating MT. This pathway could explain the persistence of motion sensitivity in subjects following injury to V1, suggesting more generally that residual perception after damage in a primary area may arise from sparse thalamic input to 'secondary' cortical areas.

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Figure 1: Identifying a tracer injection in MT.
Figure 2: Overlap of MT-projecting neurons and tracer injections in V1.
Figure 3: MT-projecting neurons in the LGN.
Figure 4: CaMK2 immunostaining of MT-projecting neurons.

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References

  1. Riddoch, G. Dissociation of visual perceptions due to occipital injuries, with especial reference to appreciation of movement. Brain 40, 15–57 (1917).

    Article  Google Scholar 

  2. Zeki, S. & ffytche, D.H. The Riddoch syndrome: insights into the neurobiology of conscious vision. Brain 121, 25–45 (1998).

    Article  PubMed  Google Scholar 

  3. Humphrey, N.K. & Weiskrantz, L. Vision in monkeys after removal of the striate cortex. Nature 215, 595–597 (1967).

    Article  CAS  PubMed  Google Scholar 

  4. Cowey, A. & Stoerig, P. Blindsight in monkeys. Nature 373, 247–249 (1995).

    Article  CAS  PubMed  Google Scholar 

  5. Stoerig, P. & Cowey, A. Blindsight in man and monkey. Brain 120, 535–559 (1997).

    Article  PubMed  Google Scholar 

  6. Newsome, W.T., Britten, K.H. & Movshon, J.A. Neuronal correlates of a perceptual decision. Nature 341, 52–54 (1989).

    Article  CAS  PubMed  Google Scholar 

  7. Salzman, C.D., Murasugi, C.M., Britten, K.H. & Newsome, W.T. Microstimulation in visual area MT: effects on direction discrimination performance. J. Neurosci. 12, 2331–2355 (1992).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Watson, J.D. et al. Area V5 of the human brain: evidence from a combined study using positron emission tomography and magnetic resonance imaging. Cereb. Cortex 3, 79–94 (1993).

    Article  CAS  PubMed  Google Scholar 

  9. Beckers, G. & Zeki, S. The consequences of inactivating areas V1 and V5 on visual motion perception. Brain 118, 49–60 (1995).

    Article  PubMed  Google Scholar 

  10. Zeki, S.M. The secondary visual areas of the monkey. Brain Res. 13, 197–226 (1969).

    Article  CAS  PubMed  Google Scholar 

  11. Cragg, B.G. The topography of the afferent projections in the circumstriate visual cortex of the monkey studied by the Nauta method. Vision Res. 9, 733–747 (1969).

    Article  CAS  PubMed  Google Scholar 

  12. Zeki, S. & Shipp, S. The functional logic of cortical connections. Nature 335, 311–317 (1988).

    Article  CAS  PubMed  Google Scholar 

  13. Felleman, D.J. & Van Essen, D.C. Distributed hierarchical processing in the primate cerebral cortex. Cereb. Cortex 1, 1–47 (1991).

    Article  CAS  PubMed  Google Scholar 

  14. Yukie, M. & Iwai, E. Direct projection from the dorsal lateral geniculate nucleus to the prestriate cortex in macaque monkeys. J. Comp. Neurol. 201, 81–97 (1981).

    Article  CAS  PubMed  Google Scholar 

  15. Fries, W. The projection from the lateral geniculate nucleus to the prestriate cortex of the macaque monkey. Proc. R. Soc. Lond. B 213, 73–86 (1981).

    Article  CAS  PubMed  Google Scholar 

  16. Lysakowski, A., Standage, G.P. & Benevento, L.A. An investigation of collateral projections of the dorsal lateral geniculate nucleus and other subcortical structures to cortical areas V1 and V4 in the macaque monkey: a double label retrograde tracer study. Exp. Brain Res. 69, 651–661 (1988).

    Article  CAS  PubMed  Google Scholar 

  17. Bullier, J. & Kennedy, H. Projection of the lateral geniculate nucleus onto cortical area V2 in the macaque monkey. Exp. Brain Res. 53, 168–172 (1983).

    Article  CAS  PubMed  Google Scholar 

  18. Benevento, L.A. & Yoshida, K. The afferent and efferent organization of the lateral geniculo-prestriate pathways in the macaque monkey. J. Comp. Neurol. 203, 455–474 (1981).

    Article  CAS  PubMed  Google Scholar 

  19. Horton, J.C. Cytochrome oxidase patches: a new cytoarchitectonic feature of monkey visual cortex. Phil. Trans. R. Soc. Lond. B 304, 199–253 (1984).

    Article  CAS  Google Scholar 

  20. Stepniewska, I., Qi, H.X. & Kaas, J.H. Do superior colliculus projection zones in the inferior pulvinar project to MT in primates? Eur. J. Neurosci. 11, 469–480 (1999).

    Article  CAS  PubMed  Google Scholar 

  21. Yoshida, K. & Benevento, L.A. The projection from the dorsal lateral geniculate nucleus of the thalamus to extrastriate visual association cortex in the macaque monkey. Neurosci. Lett. 22, 103–108 (1981).

    Article  CAS  PubMed  Google Scholar 

  22. Benevento, L.A. & Standage, G.P. Demonstration of lack of dorsal lateral geniculate nucleus input to extrastriate areas MT and Visual 2 in the macaque monkey. Brain Res. 252, 161–166 (1982).

    Article  CAS  PubMed  Google Scholar 

  23. Sorenson, K.M. & Rodman, H.R. A transient geniculo-extrastriate pathway in macaques? Implications for 'blindsight'. Neuroreport 10, 3295–3299 (1999).

    Article  CAS  PubMed  Google Scholar 

  24. Tong, F. Primary visual cortex and visual awareness. Nat. Rev. Neurosci. 4, 219–229 (2003).

    Article  CAS  PubMed  Google Scholar 

  25. Crick, F. & Koch, C. A framework for consciousness. Nat. Neurosci. 6, 119–126 (2003).

    Article  CAS  PubMed  Google Scholar 

  26. Sincich, L.C. & Horton, J.C. Independent projection streams from macaque striate cortex to the second visual area and middle temporal area. J. Neurosci. 23, 5684–5692 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Shipp, S. & Zeki, S. The organization of connections between areas V5 and V1 in macaque monkey visual cortex. Eur. J. Neurosci. 1, 309–332 (1989).

    Article  CAS  PubMed  Google Scholar 

  28. Yukie, M. & Iwai, E. Laminar origin of direct projection from cortex area V1 to V4 in the rhesus monkey. Brain Res. 346, 383–386 (1985).

    Article  CAS  PubMed  Google Scholar 

  29. Ungerleider, L.G. & Mishkin, M. The striate projection zone in the superior temporal sulcus of Macaca mulatta: location and topographic organization. J. Comp. Neurol. 188, 347–366 (1979).

    Article  CAS  PubMed  Google Scholar 

  30. Hendry, S.H. & Yoshioka, T. A neurochemically distinct third channel in the macaque dorsal lateral geniculate nucleus. Science 264, 575–577 (1994).

    Article  CAS  PubMed  Google Scholar 

  31. Rodman, H.R., Sorenson, K.M., Shim, A.J. & Hexter, D.P. Calbindin immunoreactivity in the geniculo-extrastriate system of the macaque: implications for heterogeneity in the koniocellular pathway and recovery from cortical damage. J. Comp. Neurol. 431, 168–181 (2001).

    Article  CAS  PubMed  Google Scholar 

  32. Malpeli, J.G. & Baker, F.H. The representation of the visual field in the lateral geniculate nucleus of Macaca mulatta. J. Comp. Neurol. 161, 569–594 (1975).

    Article  CAS  PubMed  Google Scholar 

  33. Hendry, S.H. & Reid, R.C. The koniocellular pathway in primate vision. Annu. Rev. Neurosci. 23, 127–153 (2000).

    Article  CAS  PubMed  Google Scholar 

  34. Saito, H., Tanaka, K., Isono, H., Yasuda, M. & Mikami, A. Directionally selective response of cells in the middle temporal area (MT) of the macaque monkey to the movement of equiluminous opponent color stimuli. Exp. Brain Res. 75, 1–14 (1989).

    Article  CAS  PubMed  Google Scholar 

  35. Seidemann, E., Poirson, A.B., Wandell, B.A. & Newsome, W.T. Color signals in area MT of the macaque monkey. Neuron 24, 911–917 (1999).

    Article  CAS  PubMed  Google Scholar 

  36. Callaway, E.M. Local circuits in primary visual cortex of the macaque monkey. Annu. Rev. Neurosci. 21, 47–74 (1998).

    Article  CAS  PubMed  Google Scholar 

  37. Raiguel, S.E., Lagae, L., Gulyas, B. & Orban, G.A. Response latencies of visual cells in macaque areas V1, V2 and V5. Brain Res. 493, 155–159 (1989).

    Article  CAS  PubMed  Google Scholar 

  38. Schmolesky, M.T. et al. Signal timing across the macaque visual system. J. Neurophysiol. 79, 3272–3278 (1998).

    Article  CAS  PubMed  Google Scholar 

  39. Nowak, L.G. & Bullier, J. The timing of information transfer in the visual system. in Cerebral Cortex (eds. K.S. Rockland, J.H. Kaas & A. Peters) 205–241 (Plenum, New York, 1997).

    Google Scholar 

  40. Maunsell, J.H. & Gibson, J.R. Visual response latencies in striate cortex of the macaque monkey. J. Neurophysiol. 68, 1332–1344 (1992).

    Article  CAS  PubMed  Google Scholar 

  41. Nowak, L.G., Munk, M.H., Girard, P. & Bullier, J. Visual latencies in areas V1 and V2 of the macaque monkey. Vis. Neurosci. 12, 371–384 (1995).

    Article  CAS  PubMed  Google Scholar 

  42. Cropper, S.J. & Derrington, A.M. Rapid colour-specific detection of motion in human vision. Nature 379, 72–74 (1996).

    Article  CAS  PubMed  Google Scholar 

  43. Rodman, H.R., Gross, C.G. & Albright, T.D. Afferent basis of visual response properties in area MT of the macaque. I. Effects of striate cortex removal. J. Neurosci. 9, 2033–2050 (1989).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Girard, P., Salin, P.A. & Bullier, J. Response selectivity of neurons in area MT of the macaque monkey during reversible inactivation of area V1. J. Neurophysiol. 67, 1437–1446 (1992).

    Article  CAS  PubMed  Google Scholar 

  45. Barbur, J.L., Watson, J.D., Frackowiak, R.S. & Zeki, S. Conscious visual perception without V1. Brain 116, 1293–1302 (1993).

    Article  PubMed  Google Scholar 

  46. Collins, C.E., Lyon, D.C. & Kaas, J.H. Responses of neurons in the middle temporal visual area after long-standing lesions of the primary visual cortex in adult new world monkeys. J. Neurosci. 23, 2251–2264 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Rodman, H.R., Gross, C.G. & Albright, T.D. Afferent basis of visual response properties in area MT of the macaque. II. Effects of superior colliculus removal. J. Neurosci. 10, 1154–1164 (1990).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Stepniewska, I., Ql, H.X. & Kaas, J.H. Projections of the superior colliculus to subdivisions of the inferior pulvinar in New World and Old World monkeys. Vis. Neurosci. 17, 529–549 (2000).

    Article  CAS  PubMed  Google Scholar 

  49. Harting, J.K., Huerta, M.F., Hashikawa, T. & van Lieshout, D.P. Projection of the mammalian superior colliculus upon the dorsal lateral geniculate nucleus: organization of tectogeniculate pathways in nineteen species. J. Comp. Neurol. 304, 275–306 (1991).

    Article  CAS  PubMed  Google Scholar 

  50. Maunsell, J.H., Nealey, T.A. & DePriest, D.D. Magnocellular and parvocellular contributions to responses in the middle temporal visual area (MT) of the macaque monkey. J. Neurosci. 10, 3323–3334 (1990).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We thank K.D. Murray for advice on CaMK2 immunochemistry and J. Kaas for comments on the manuscript. The work was supported by The Larry L. Hillblom Foundation and by National Eye Institute grants (to L.C.S., J.C.H.) and the Beckman Vision Center. The California Regional Primate Research Center was supported by a National Institutes of Health Base Grant.

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  1. Beckman Vision Center, University of California, 10 Koret Way, San Francisco, 94143, California, USA

    Lawrence C Sincich, Ken F Park, Melville J Wohlgemuth & Jonathan C Horton

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Correspondence to Lawrence C Sincich.

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Supplementary information

Supplementary Fig. 1

Tracer injection in area MT did not contaminate cortical white matter. Displayed are the remaining CO-CTB reacted sections from the right hemisphere of Monkey 1, in a continuous series from the section shown in Figure 1 down to white matter. The same location is indicated by the red arrow in all sections. Note that by section 17, only white matter is visible and the injection bolus is no longer present. The possibility of white matter contamination is a significant issue because the optic radiations projecting from the LGN to V1 pass immediately below MT in the intact brain. Scale bar, 1 cm. (JPG 89 kb)

Supplementary Fig. 2

Microphotographs of the LGN sections used for camera lucida plots in Figure 2. At this magnification, only the clusters of WGA-HRP labeled cells are visible, though these sections were reacted for both CTB and WGA-HRP. Scale bar, 1 mm. (JPG 47 kb)

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Sincich, L., Park, K., Wohlgemuth, M. et al. Bypassing V1: a direct geniculate input to area MT. Nat Neurosci 7, 1123–1128 (2004). https://doi.org/10.1038/nn1318

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