In primates,the pathway mediating visual perception passes from the
retina via the LGN to V1.From V1,output is distributed to a panoply
of higher extrastriate cortical areas. Historically, these regions were
defined as ‘higher’ because they were not thought to receive direct
geniculate input.In humans,loss of V1 devastates eyesight by cutting
off the flow of visual information from the LGN to extrastriate visual
cortex. Curiously, patients affected by such lesions manifest residual
perception—notably for moving stimuli—which occurs either con-
sciously (Riddoch syndrome)1,2or unconsciously (blindsight)3,4.
This phenomenon has engendered considerable controversy5, and
even skepticism,because it defies conventional ideas about the organ-
ization of the visual system.
Area MT is a likely site to mediate the persistent ability to sense
motion after damage to area V1. In macaques, the responses of single
cells in MT account for perceptual decisions about the direction of
moving stimuli6. Moreover, such judgments are influenced by electri-
cal stimulation,implying direct participation by MT in the perception
of motion7. A motion-selective area that is homologous to MT has
been located in humans8and is vital to motion perception9. Because
MT receives a substantial direct projection from V1 (refs.10,11),it has
been placed directly above V1 in hierarchical models of the visual sys-
tem12,13. Such models currently provide the basic structural frame-
work for explaining neurological syndromes affecting vision.
The simplest explanation for motion sensitivity in subjects after V1
loss is that a visual pathway exists that bypasses V1 to reach MT.Such
a pathway might be sufficient to sustain crude motion perception
after destruction ofV1.Numerous investigators have sought evidence
that the LGN projects directly to extrastriate cortex. Indeed, after
tracer injection into V2 and V4,scattered retrogradely filled cells have
been described in the LGN14–18. In a few studies, a direct projection
from LGN to MT has also been reported15,19,20. These studies have
relied on observations in only a few animals, however, and have been
contradicted by negative findings21–23. An important technical con-
cern is that the optic radiations pass immediately underneath MT,
creating the potential for artifactual labeling of LGN cells by tracer
leakage into the white matter. In addition, MT in macaques is com-
pletely buried in the superior temporal sulcus (STS),and it lacks well-
defined cytoarchitectonic boundaries. These factors make it
challenging to place tracer injections accurately into MT without
spillover into surrounding cortical areas. Thus a definitive verdict
about the existence of projections from LGN to MT is needed.
Settling the issue has become especially desirable because MT and V1
are often cast as ‘generic’ cortical areas in neuroscience, serving as
exemplars for studies of cortical processing,perceptual cognition and
even conscious awareness24,25.
To re-examine this issue, we made anatomically verified injections
confined to MT in the macaque monkey.We found a sizable popula-
tion of retrogradely labeled neurons in the LGN that provide direct
input to MT.Immunostaining showed that the majority of these neu-
rons form part of the koniocellular system.Notably,a novel subpopu-
lation was present in the LGN intercalated layers, unrelated to the
koniocellular system. Our results indicate that a specialized pathway
exists from the LGN to MT, which may carry unique visual signals to
the motion area in primates.
Distribution of MT-projecting neurons in the LGN and V1
To establish the existence of a direct projection from the LGN to MT,
we used a retrograde tracing technique (with CTB, gold-conjugated
cholera toxin B subunit) in conjunction with a method of physically
unfolding the cortical tissue to delineate clearly area MT26. We also
verified that the tracer was deposited exclusively in MT by examining
the distribution of retrogradely labeled cells in area V1. To indicate
how deeply buried MT is in the STS, we show a lateral view of the
right hemisphere of monkey 1 at an early stage in the unfolding pro-
cedure (Fig. 1a). The STS is opened to reveal the location of a single
CTB injection in the posterior bank where MT is situated. We also
made an array of injections of a second retrograde tracer,WGA-HRP
(wheat-germ agglutinin conjugated to horseradish peroxidase) in
area V1. The purpose of these additional injections was to ascertain
Beckman Vision Center, University of California, 10 Koret Way, San Francisco, California 94143, USA. Correspondence should be addressed to L.C.S.
Published online 19 September 2004; doi:10.1038/nn1318
Bypassing V1: a direct geniculate input to area MT
Lawrence C Sincich,Ken F Park,Melville J Wohlgemuth & Jonathan C Horton
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 (MT or 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.
NATURE NEUROSCIENCE VOLUME 7 | NUMBER 10 | OCTOBER 2004
© 2004 Nature Publishing Group http://www.nature.com/natureneuroscience
VOLUME 7 | NUMBER 10 | OCTOBER 2004 NATURE NEUROSCIENCE
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).
12. Zeki, S. & Shipp, S. The functional logic of cortical connections. Nature 335,
13. Felleman, D.J. & Van Essen, D.C. Distributed hierarchical processing in the primate
cerebral cortex. Cereb. Cortex 1, 1–47 (1991).
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).
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).
16. Lysakowski, A., Standage, G.P. & Benevento, L.A. An investigation of collateral pro-
jections 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).
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).
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,
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).
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
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 mon-
key. Neurosci. Lett. 22, 103–108 (1981).
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).
23. Sorenson, K.M. & Rodman, H.R. A transient geniculo-extrastriate pathway in
macaques? Implications for ‘blindsight’. Neuroreport 10, 3295–3299 (1999).
24. Tong, F. Primary visual cortex and visual awareness. Nat. Rev. Neurosci. 4, 219–229
25. Crick, F. & Koch, C. A framework for consciousness. Nat. Neurosci. 6, 119–126 (2003).
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,
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).
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).
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).
30. Hendry, S.H. & Yoshioka, T. A neurochemically distinct third channel in the macaque
dorsal lateral geniculate nucleus. Science 264, 575–577 (1994).
31. Rodman, H.R., Sorenson, K.M., Shim, A.J. & Hexter, D.P. Calbindin immunoreactiv-
ity 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).
32. Malpeli, J.G. & Baker, F.H. The representation of the visual field in the lateral genic-
ulate nucleus of Macaca mulatta. J. Comp. Neurol. 161, 569–594 (1975).
33. Hendry, S.H. & Reid, R.C. The koniocellular pathway in primate vision. Annu. Rev.
Neurosci. 23, 127–153 (2000).
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).
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).
36. Callaway, E.M. Local circuits in primary visual cortex of the macaque monkey. Annu.
Rev. Neurosci. 21, 47–74 (1998).
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).
38. Schmolesky, M.T. et al. Signal timing across the macaque visual system.
J. Neurophysiol. 79, 3272–3278 (1998).
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
40. Maunsell, J.H. & Gibson, J.R. Visual response latencies in striate cortex of the
macaque monkey. J. Neurophysiol. 68, 1332–1344 (1992).
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).
42. Cropper, S.J. & Derrington, A.M. Rapid colour-specific detection of motion in human
vision. Nature 379, 72–74 (1996).
43. Rodman, H.R., Gross, C.G. & Albright, T.D. Afferent basis of visual response proper-
ties in area MT of the macaque. I. Effects of striate cortex removal. J. Neurosci. 9,
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,
45. Barbur, J.L., Watson, J.D., Frackowiak, R.S. & Zeki, S. Conscious visual perception
without V1. Brain 116, 1293–1302 (1993).
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).
47. Rodman, H.R., Gross, C.G. & Albright, T.D. Afferent basis of visual response proper-
ties in area MT of the macaque. II. Effects of superior colliculus removal.
J. Neurosci. 10, 1154–1164 (1990).
48. Stepniewska, I., Ql, H.X. & Kaas, J.H. Projections of the superior colliculus to subdi-
visions of the inferior pulvinar in New World and Old World monkeys. Vis. Neurosci.
17, 529–549 (2000).
49. Harting, J.K., Huerta, M.F., Hashikawa, T. & van Lieshout, D.P. Projection of the mam-
malian superior colliculus upon the dorsal lateral geniculate nucleus: organization of
tectogeniculate pathways in nineteen species. J. Comp. Neurol. 304, 275–306 (1991).
50. Maunsell, J.H., Nealey, T.A. & DePriest, D.D. Magnocellular and parvocellular con-
tributions to responses in the middle temporal visual area (MT) of the macaque mon-
key. J. Neurosci. 10, 3323–3334 (1990).
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