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Topographical and topological organization of the thalamocortical projection to the striate and prestriate cortex in the marmoset (Callithrix jacchus)

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Summary

In eleven hemispheres of nine marmoset monkeys (Callithrix jacchus), we have investigated the thalamo-cortical organization of the projections from the pulvinar to the striate and prestriate cortex. In each experiment, single or multiple injections of various retrograde fluorescent tracers were injected into adjacent regions or areas. In two experiments, horseradish peroxidase (HRP) was injected into the lateral geniculate nucleus (LGN) and the lateral pulvinar, respectively. The results show that the thalamo-cortical projection from LGN to striate cortex and from pulvinar to the prestriate cortex are similarly organized, but the geniculo-striate projection is more precise than the pulvinar-prestriate projection. The pulvinar-prestriate projection is topographically organized and preserves topological neighbourhood relations. Projection zones to the various visual areas are concentrically wrapped around each other. The projection zone to area 18 constitutes a central core region. It begins ventro-laterally in PuL where the pulvinar is in contact with the LGN. This contact zone we called the hilus region of the pulvinar. The area 18-projection zone stretches as a central cone into the posterior pulvinar through PuL and into PuM. It is surrounded by the projection zone to the posterior belt of area 19 and this in turn is surrounded by the projection zone to the anterior belt of area 19. The projection zones to area 19 are then surrounded medially and dorsally by zones projectiong to the temporal and parietal association cortex, respectively. The projection zone to area MT is located medio-ventrally in the posterior pulvinar (PuIP and surrounding nuclei) and coincides with a densely myelinated region. Area 17 also receives input from the pulvinar but probably predominantly in the region of the central visual field. The pulvinar zone projecting to area 17 is located ventrolaterally from the central core region projecting to area 18 and is contiguous laterally with the LGN. If the positions of the vertical and the horizontal meridian in the pulvinar correspond to those in the respective cortical projection zones, a second order visual field representation such as found in area 18, with the horizontal meridian split at an excentricity of about 7–10°, can also be recognized in the pulvinar.

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Abbreviations

A :

Subcortical nuclei and subnuclei, cf. — Stephan et al. (1980)

AD:

Nucleus anterior dorsalis thalami

AV:

Nucleus anterior ventralis thalami

CeD:

Nucleus centralis dorsalis thalami

CeL:

Nucleus centralis lateralis thalami

CeMe:

Centrum medianum thalami

CoS:

Colliculus superior

FRPO:

Formatio reticularis pontis, pars oralis

GM:

Corpus geniculatum mediale

IBCI:

Nucleus interstitialis brachii colliculi inferioris

LGN:

Corpus geniculatum laterale dorsale

vLGN:

Corpus geniculatum laterale ventrale

LD:

Nucleus lateralis dorsalis thalami

LI:

Nucleus limitans thalami

LP:

Nucleus lateralis posterior thalami

MD:

Nucleus medialis dorsalis thalami

OL:

Nucleus olivaris superior lateralis

OM:

Nucleus olivaris superior medialis

Pbg:

Nucleus parabigeminalis

Pul:

Pulvinar inferior; PulP Pulvinar inferior posterior

PuL:

Pulvinar lateralis

PuM:

Pulvinar medialis

PuO:

Pulvinar oralis

RT:

Nucleus reticularis thalami

Sg:

Nucleus suprageniculatus

VA:

Nucleus ventralis anterior thalami

VL:

Nucleus ventralis lateralis thalami

VPL:

Nucleus ventralis posterior lateralis thalami

VPM:

Nucleus ventralis posterior medialis thalami

IV:

Nucleus nervi trochlearis

B :

Cortical areas and subareas, (after Spatz 1977a; Spatz et al. 1987 Allman and Kaas 1975):

17:

Area striata (V I)

18:

Area 18 (V II)

19DI:

Area 19 dorso-intermediate

19DL:

Area 19 dorso-lateral

19DM:

Area 19 dorso-medial

19M:

Area 19 medial

19V:

Area 19 ventral

MT:

Middle temporal area

References

  1. Albus K, Beckmann R (1980) Second and third visual areas of the cat: interindividual variability in retinotopic arrangement and cortical location. J Physiol 299:247–276

  2. Allman JM, Kaas JH (1971) A representation of the visual field in the caudal third of the middle temporal gyrus of the owl monkey (Aotus trivirgatus). Brain Res 31:85–105

  3. Allman JM, Kaas JH, Lane RH, Miezin FM (1972) A representation of the visual field in the inferior nucleus of the pulvinar in the owl monkey (Aotus trivirgatus). Brain Res 40:291–302

  4. Allman JM, Kaas JH (1974) The organization of the second visual area (V II) in the owl monkey: a second order transformation of the visual hemifield. Brain Res 76:247–265

  5. Allman JM, Kaas JH (1975) The dorsomedial cortical visual area: a third tier area in the occipital lobe of the owl monkey (Aotus trivirgatus). Brain Res 100:473–487

  6. Allman JM, Baker JF, Newsome WT, Petersen ST (1981) Visual topography and function. In: Woolsey CN (eds) Cortical sensory organisation, Vol 2. Multiple visual areas. Humana Press, Clifton NJ, pp 171–185

  7. Aschoff A, Holländer H (1982) Fluorescent compounds as retrograde tracers compared with horseradish peroxidase (HRP). I. A parametric study in the central visual system of the albino rat. J Neurosci Meth 6:179–197

  8. Baker JF, Petersen SE, Newsome WT, Allman JM (1981) Visual response properties of neurons in four extrastriate visual areas of the owl monkey (Aotus trivirgatus): a quantitative comparison of medial, dorsomedial, dorsolateral, and middle temporal areas. J Neurophysiol 3:397–416

  9. Bender DB (1981) Retinotopic organization of macaque pulvinar. J Neurophysiol 3:672–693

  10. Benedek G, Norita M, Creutzfeldt OD (1983) Electrophysiological and anatomical demonstration of an overlapping striate and tectal projection to the lateral posterior-pulvinar complex of the cat. Exp Brain Res 52:157–169

  11. Benevento LA, Fallon JH (1975) The ascending projections of the superior colliculus in the rhesus monkey (Macaca mulatta). J Comp Neurol 160:339–362

  12. Benevento LA, Rezak M (1975) Extrageniculate projections to layers VI and I of striate cortex (area 17) in the rhesus monkey (Macaca mulatta). Brain Res 96:51–55

  13. Benevento LA, Rezak M (1976) The cortical projections of the inferior pulvinar and adjacent lateral pulvinar in the rhesus monkey (Macaca mulatta): an autoradiographic study. Brain Res 108:1–24

  14. Benevento LA, Standage GP (1983) The organization of projections of the retinorecipient and nonretinorecipient nuclei of the pretectal complex and layers of the superior colliculus to the lateral pulvinar and medial pulvinar in the macaque monkey. J Comp Neurol 217:307–336

  15. Brodmann K (1909) Vergleichende Lokalisationslehre der Großhirnrinde. J. A. Barth, Leipzig

  16. Brysch I, Creutzfeldt O, Hayes NL, Schlingensiepen KH (1984) The second intralaminar thalamo-cortical projection system. Anat Embryol 169:111–118

  17. Brysch W, Brysch I, Creutzfeldt OD, Schlingensiepen R, Schlingensiepen KH (1990) The topology of the thalamo-cortical projections in the marmoset. Exp Brain Res 81:1–17

  18. Carey RG, Fitzpatrick D, Diamond IT (1979a) Thalamic projections to layer I of striate cortex shown by retrograde transport of horseradish peroxidase. Science 203:556–558

  19. Carey RG, Fitzpatrick D, Diamond IT (1979b) Layer I of striate cortex of Tupaia glis and Galago senegalensis: projections from thalamus and claustrum revealed by retrograde transport of horseradish peroxidase. J Comp Neurol 186:393–438

  20. Creutzfeldt OD (1985) Comparative aspects of representation in the visual system. Exp Brain Res Suppl 11:53–81

  21. DeVito JL (1978) A horseradish peroxidase-autoradiographic study of parietopulvinar connections in Saimiri sciureus. Exp Brain Res 32:581–590

  22. Donaldson IML, Whitteridge D (1977) The nature of the boundary between cortical visual areas II and III in the cat. Proc R Soc B 199:445–462

  23. Doty RW, Kimura DS, Mogenson GJ (1964) Photically and electrically elicited responses in the central visual system of the squirrel monkey. Exp Neurol 10:19–51

  24. Doty RW (1983) Nongeniculate afferents to striate cortex in macaques. J Comp Neurol 218:159–173

  25. Gallyas F (1979) Silver staining of myelin by means of physical development. Neurol Res 1:203–209

  26. Glendenning KK, Hall JA, Diamond IT, Hall WC (1975) The pulvinar nucleus of Galago senegalensis. J Comp Neurol 161:419–458

  27. Graybiel AM, Berson DM (1980) Histochemical identification and afferent connections of subdivisions in the lateralis posteriorpulvinar complex and related thalamic nuclei in the cat. Neuroscience 5:1175–1238

  28. Guedes R, Watanabe S, Creutzfeldt OD (1983) Functional role of association fibres for a visual association area: the posterior suprasylvian sulcus of the cat. Exp Brain Res 49:13–27

  29. Harting JK, Hall WC, Diamond IT (1972) Evolution of the pulvinar. Brain Behav Evol 6:424–452

  30. Harting JK, Huerta MF, Frankfurter AJ, Strominger NL, Royce GJ (1980) Ascending pathways from the monkey superior colliculus: an autoradiographic analysis. J Comp Neurol 192:853–882

  31. Illert M, Fritz N, Aschoff A, Holländer H (1982) Fluorescent compounds as retrograde tracers compared with horseradish peroxidase (HRP). II. A parametric study in the peripheral motor system of the cat. J Neurosci Meth 6:199–218

  32. Jones EG (1985) Comparative anatomy of the thalamus. In: The thalamus, Chap 10. Plenum Press, New York London, pp529–604

  33. Kaske A, Dick A, Creutzfeldt OD (1991) The local domain for divergence of subcortical afferents to the striate and extrastriate visual cortex in the common marmoset (Callithrix jacchus): a multiple labelling study. Exp Brain Res 84:254–265

  34. Katz LC, Burkhalter A, Dreyer WJ (1984) Fluorescent latex microspheres as a retrograde neuronal marker for in vivo and in vitro studies of visual cortex. Nature 310:498–500

  35. Keizer K, Kuypers HGJM, Huisman AM, Danny O (1983) Diamidino yellow dihydrochloride (DY 2HCl), a new fluorescent retrograde neuronal tracer, which migrates only very slowly out of the cell. Exp Brain Res 51:179–191

  36. Kennedy H, Bullier J (1985) A double-labeling investigation of the afferent connectivity to cortical areas V1 and V2 of the macaque monkey. J Neurosci 10:2815–2830

  37. Kuypers HGJM, Bentivoglio M, Catsman-Berrevoets CE, Bharos AT (1980) Double retrograde neuronal labeling through divergent axon collaterals, using two fluorescent tracers with the same excitation wavelength which label different features of the cell. Exp Brain Res 40:383–392

  38. Lin CS, Kaas JH (1979) The inferior pulvinar complex in owl monkeys: architectonic subdivisions and patterns of input from the superior colliculus and subdivisions of visual cortex. J Comp Neurol 187:655–678

  39. Lin CS, Kaas JH (1980) Projections from the medial nucleus of the inferior pulvinar complex to the middle temporal area of the visual cortex. Neuroscience 5:2219–2228

  40. Livingstone M, Hubel D (1989) Segregation of form, color, movement, and depth: anatomy, physiology, and perception. Science 240:740–749

  41. Lund JS, Lund RD, Hendricksen AE, Bunt AH, Fuchs AF (1975) The origin of efferent pathways from the primary visual cortex, area 17, of the macaque monkey as shown by retrograde transport of horseradish peroxidase. J Comp Neurol 164:287–304

  42. Lysakowski A, Standage GP, Benevento LA (1986) Histochemical and architectonic differentiation of zones of pretectal and collicular inputs to the pulvinar and dorsal lateral geniculate nuclei in the macaque. J Comp Neurol 250:431–448

  43. Mesulam MM (1978) Tetramethyl benzidine for horseradish peroxidase neurohistochemistry: a non-carcinogenic blue reaction product with superior sensitivity for visualizing neural afferents and efferents. J Histochem Cytochem 26:106–117

  44. Niimi K, Kuwahara E (1973) The dorsal thalamus of the cat and comparison with monkey and man. J Hirnforsch 14:303–325

  45. Ogren MP, Hendrickson AE (1977) The distribution of pulvinar terminals in visual areas 17 and 18 of the monkey. Brain Res 137:343–350

  46. Peden JK, von Bonin G (1947) The neocortex of Hapale. J Comp Neurol 86:37–64

  47. Petersen SE, Robinson DL, Keys W (1985) Pulvinar nuclei of the behaving rhesus monkey: visual responses and their modulation. J Neurophysiol 4:397–416

  48. Raczkowski D, Diamond IT (1980) Cortical connections of the pulvinar nucleus in Galago. J Comp Neurol 193:1–40

  49. Raczkowski D, Diamond IT (1981) Projections from the superior colliculus and the neocortex to the pulvinar nucleus in Galago. J Comp Neurol 200:231–254

  50. Rezak M, Benevento LA (1979) A comparison of the organization of the projections of the dorsal lateral geniculate nucleus, the inferior pulvinar and adjacent lateral pulvinar to primary visual cortex (area 17) in the macaque monkey. Brain Res 167:19–40

  51. Schmued LC, Fallon JH (1986) Fluoro-gold: a new fluorescent retrograde axonal tracer with numerous unique properties. Brain Res 377:147–154

  52. Spatz WB, Tigges J (1972) Experimental-anatomical studies on the “middle temporal visual area (MT)” in primates. I. Efferent cortico-cortical connections in the marmoset Callithrix jacchus. J Comp Neurol 146:451–464

  53. Spatz WB (1977a) Der visuelle Bereich der Großhirnrinde: experimentell-anatomische Untersuchungen zu seiner Gliederung und der ipsilateralen Assoziationsverbindungen bei Callithrix jacchus. Habilitationsschrift. Med. Fakultät, Johann-Wolfgang-Goethe Universität, Frankfurt/Main

  54. Spatz WB (1977b) Topographically organized reciprocal connections between areas 17 and MT (visual area of superior temporal sulcus) in the marmoset Callithrix jacchus. Exp Brain Res 27:559–572

  55. Spatz WB, Kunz B, Steffen H (1987) A new heterotopic callosal projection of primary visual cortex in the monkey, Callithrix jacchus. Brain Res 403:158–161

  56. Standage GP, Benevento LA (1983) The organization of connections between the pulvinar and visual area MT in the macaque monkey. Brain Res 262:288–294

  57. Stephan H, Baron G, Schwerdtfeger WK (1980) The brain of the common marmoset: a stereotaxic atlas. Springer, Berlin Heidelberg New York

  58. Storm-Mathisen J (1970) Quantitative histochemistry of acetylcholinesterase in rat hippocampal region correlated to histochemical staining. J Neurochem 17:739–750

  59. Symonds LL, Kaas JH (1978) Connections of striate cortex in the prosimian, Galago senegalensis. J Comp Neurol 181:477–512

  60. Tanaka M, Lindsley E, Lausmann S, Creutzfeldt OD (1990) Afferent connections of the prelunate visual association cortex (areas V4 and DP). Anat Embryol 181:19–30

  61. Tanaka M, Weber H, Creutzfeldt OD (1986) Visual properties and spatial distribution of neurones in the visual association area on the prelunate gyrus of the awake monkey. Exp Brain Res 65:11–37

  62. Tootell RBH, Hamilton SL, Silverman MS (1985) Topography of cytochrome oxidase activity in owl monkey cortex. J Neurosci 10:2786–2800

  63. Trojanowski JQ, Jacobson S (1975) A combined horseradish peroxidase-autoradiographic investigation of reciprocal connections between superior temporal gyrus and pulvinar in squirrel monkey. Brain Res 85:347–353

  64. Ungerleider LG, Galkin TW, Mishkin M (1983) Visuotopic organization of projections from striate cortex to inferior and lateral pulvinar in rhesus monkey. J Comp Neurol 217:137–157

  65. Weller RE, Kaas JH (1981) Cortical and subcortical connections of visual cortex in primates. In: Woolsey CN (eds) Cortical sensory organization. 2. Multiple visual areas. Humana Press, Clifton NJ, pp 121–156

  66. Wong-Riley MTT (1977) Connections between the pulvinar nucleus and the prestriate cortex in the squirrel monkey as revealed by peroxidase histochemistry and autoradiography. Brain Res 134:225–236

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Correspondence to O. D. Creutzfeldt.

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Dick, A., Kaske, A. & Creutzfeldt, O.D. Topographical and topological organization of the thalamocortical projection to the striate and prestriate cortex in the marmoset (Callithrix jacchus). Exp Brain Res 84, 233–253 (1991). https://doi.org/10.1007/BF00231444

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Key words

  • Pulvinar
  • Area 17
  • Prestriate cortex
  • Thalamo-cortical organization
  • Callithrix jacchus