Skip to main content

Topographical projections of the prestriate cortex to the pulvinar nuclei in the macaque monkey: An autoradiographic study

Experimental Brain Research volume 30, pages 405–424 (1977)Cite this article

Summary

Localized microinjections of tritiated amino acids were made in the prestriate cortex (areas 18 and 19) of macaque monkeys in order to determine the topography of the subcortical projections. It was found that the prestriate cortex projected to the entire inferior pulvinar (PI), lateral pulvinar (PL), dorsolateral nucleus, the lateral posterior nucleus, the reticular nucleus, a portion of the medial pulvinar, superior colliculus, and caudate nucleus but not to the dorsal lateral geniculate nucleus. The projections to the PI were organized according to the topographical representation of the contralateral visual hemifield. The ventral portion of the PL which is immediately adjacent to the PI also received a parallel topographical projection in register with the representation of the visual hemifield and thus is distinguished from the remainder of the PL. The dorsal and caudal portions of the PL (which extend to form the lateral portion of the caudal pole of the pulvinar and are located away from PI) also received projections from prestriate cortex which often appeared as several bands of grains. However, although dorsal prestriate cortex seemed to project to the dorsal portion of caudal PL and ventral prestriate cortex seemed to project to the ventral portion of caudal PL, any further topography in the projections to the dorsal and caudal PL as well as any to the other dorsal group nuclei was difficult to determine. The results point to the conclusion that the PI and the immediately adjacent portion of PL are distinguished from the remainder of the pulvinar by their connectional organization, and each region contains a representation of the visual hemifield. Furthermore, the prestriate projections to these and other regions of the pulvinar form the corticothalamic half of visual and visuomotor cortico-thalamocortical projections which involve all the occipital cortices (areas 17, 18 and 19) as well as inferotemporal, parietal and frontal cortices.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

Price includes VAT (Finland)
Tax calculation will be finalised during checkout.

Abbreviations

A:

arcuate sulcus

C:

central sulcus

Ca:

calcarine sulcus

EC:

ectocalcarine sulcus

IO:

inferior occipital sulcus

IP:

intraparietal sulcus

L:

Iunate sulcus

La:

lateral fissure

OT:

occipito-temporal sulcus

PMT:

posterior middle temporal sulcus

PO:

parieto-occipital sulcus

ST:

superior temporal sulcus

SP:

subparietal sulcus

B:

brachium of the superior colliculus

CD:

caudate nucleus

CG:

central gray

Cl:

central lateral nucleus

DL:

dorsolateral nucleus

DLG:

dorsal lateral geniculate nucleus

H:

habenular nucleus

HIP:

hippocampus

IC:

internal capsule

ICP:

principle nucleus of the inferior colliculus

Li:

limitans nucleus

MD:

dorsomedial nucleus

MG:

medial geniculate nucleus

LP:

lateral posterior nucleus

P:

pretectum

PF:

parafascicular nucleus

Pi:

inferior pulvinar

PL:

lateral pulvinar

PM:

medial pulvinar

PO:

oral pulvinar

R:

reticular nucleus

SC:

superior colliculus

Sg:

suprageniculate nucleus

VPL:

ventral posterior lateral nucleus

VPM:

ventral posterior medial nucleus

References

  • Allman, J.M., Kaas, J.H.: The organization of the second visual area (VII) in owl monkey: A second order transformation of the visual hemifield. Brain Res. 76, 247–265 (1974)

    Google Scholar 

  • Allman, J.M., Kaas, J.H.: Representation of the visual field in striate and adjoining cortex of the owl monkey (Aotus trivirgatus). Brain Res. 35, 89–106 (1971)

    Google Scholar 

  • Allman, J.M., Kaas, J.H., Iane, R.H., Miezin, F.M.: A representation of the visual field in the inferior nucleus of the pulvinar in the owl monkey (Aotus trivirgatus). Brain Res. 40, 291–302 (1972)

    Google Scholar 

  • Benevento, L.A.: Sterotaxic coordinates for the rhesus monkey thalamus and mesencephalon referencing visual afferents and cytoarchitecture. J. Hirnforsch. 16, 177–129 (1975)

    Google Scholar 

  • Benevento, L.A., Ebner, F.F.: Pretectal, tectal, retinal and cortical projections to thalamic nuclei of Virginia opossum in sterotaxic coordinates. Brain Res. 18, 171–175 (1970)

    Google Scholar 

  • Benevento, L.A., Ebner, F.F.: The areas and layers of corticocortical terminations in the visual cortex of the Virginia opossum. J. comp. Neurol. 141, 157–190 (1971)

    Google Scholar 

  • Benevento, L.A., Ebner, F.F.: The contribution of the dorsal lateral genicuIate nucleus to the total pattern of thalamic terminations in striate cortex of the Virginia opposum. J. comp. Neurol. 143, 243–260 (1971a)

    Google Scholar 

  • Benevento, L.A., Fallon, J.H.: Projection of occipital cortex to the dorsal lateral genicuIate nucleus in the rhesus monkey (Macaca muIatta). Exp. Neurol. 46, 409–417 (1975)

    Google Scholar 

  • Benevento, L.A., Fallon, J.H.: The ascending projection of the superior colliculus in the rhesus monkey (Macaca mulatta). J. comp. Neurol. 160, 339–362 (1975a)

    Google Scholar 

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

    Google Scholar 

  • Benevento, L.A., Rezak, M.: 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 (1976)

    Google Scholar 

  • Benevento, L.A., Rezak, M., Santos-Anderson, R.: An autoradiographic study of the projections of the pretectum in the rhesus monkey (Macaca mulatta): Evidence for sensorimotor links to the thalamus and oculomotor nuclei. Brain Res. 127, 197–218 (1977)

    Google Scholar 

  • Bonin, G. von, Bailey, P.: The neocortex of Macaca Mulatta. Urbana: University of Illinois Press 1947

    Google Scholar 

  • Bos, J., Benevento, L.A.: Projections of the medical pulvinar to orbital cortex and frontal eye fields in the rhesus monkey (Macaca mulatta). Exp. Neurol. 49, 487–496 (1975)

    Google Scholar 

  • Brodmann, K.: Vergleichende Lokalisationslehre der Groβhirnrinde in ihren Prinzipien dargestellt aufgrund des Zellenbaues. Leipzig: Barth 1909

    Google Scholar 

  • Burton, H., Jones, E.G.: The posterior thalamic region and its cortical projection in new world and old world monkeys. J. comp. Neurol. 168, 249–302 (1976)

    Google Scholar 

  • Campos-Ortega, J.A., Hayhow, W.R.: On the organization of the visual cortical projection to the pulvinar in Macaca muIatta. Brain Behav. Evol. 6, 394–423 (1972)

    Google Scholar 

  • Cowen, W.M., Gottlieb, D.I., Hendrickson, A., Price, J.L., Woolsey, T.A.: The autoradiographic demonstration of axonal connections in the contral nervous system. Brain Res. 37, 21–51 (1972)

    Google Scholar 

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

    Google Scholar 

  • Cynader, M., Berman, N.: Receptive-field organization of monkey superior colliculus. J. Neurophysiol. 00, 187–201 (1972)

    Google Scholar 

  • Daniel, O.M., Whitteridge, D.: The representation of the visual field on the cerebral cortex in monkeys. J. Physiol. (Lond.) 159, 203–221 (1961)

    Google Scholar 

  • Davis, B., Benevento, L.A.: Topographical projections of the prestriate cortex to the lateral pulvinar and inferior pulvinar in the macaque. Soc. Neurosci. Abstr. 2, 1074 (1976)

    Google Scholar 

  • Goldman, P.S., Nauta, W.J.H.: An intricately patterned prefrontocaudate projection in the rhesus monkey. J. comp. Neurol. 171, 360–374 (1977)

    Google Scholar 

  • Graybiel, A.M.: Some extrageniculate visual pathways in the cat. Invest. Ophthal. 11, 322–332 (1972)

    Google Scholar 

  • Holländer, H., Martinez-Millan, L.: Autoradiographic evidence for a topographically organized projection from the striate cortex to the lateral geniculate nucleus in the rhesus monkey. Brain Res. 100, 407–411 (1975)

    Google Scholar 

  • Hubel, D.H., Wiesel, T.N.: Laminar and columnar distribution of geniculo-cortical fibers in the macaque monkey. J. comp. Neurol. 146, 585–594 (1972)

    Google Scholar 

  • Jampel, R.S.: Convergence, divergence, pupillary reactions and accommodation of the eye from faradic stimulation of the macaque brain. J. comp. Neurol. 115, 371–399 (1960)

    Google Scholar 

  • Jones, E.G., Powell, T.P.S.: An anatomical study of converging sensory pathways within the cerebral cortex of the monkey. Brain 93, 783–820 (1970)

    Google Scholar 

  • Künzle, H.: Bilateral projections from precentral motor cortex to the putamen and other parts of the basal ganglia. Brain Res. 88, 195–210 (1975)

    Google Scholar 

  • Kuypers, H.G.J.M., Szwarcbart, M.K., Mishkin, M., Rosvold, H.E.: Occipito-temporal corticocortical connections in the rhesus monkey. Exp. Neurol. 11, 245–262 (1965)

    Google Scholar 

  • Lynch, J.C., Yin, T.C.T., Talbot, W.A., Mountcastle, V.B.: A cortical source of command signals for visually evoked saccadic movements of the eyes in the monkey. Soc. Neurosci. Abstr. 5, 59 (1975)

    Google Scholar 

  • Lynch, J.C., Mountcastle, V.B., Talbot, W.H., Yin, T.C.T.: Parietal lobe mechanisms for directed visual attention. J. Neurophysiol. 11, 362–389 (1977)

    Google Scholar 

  • 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)

    Google Scholar 

  • Norden, J.J., Kaas, J.H.: Some subcortical projections of the dorsomedial area (DM) of visual association cortex in the owl monkey (Aotus trivirgatus). Anat. Rec. 181, 436 (1975)

    Google Scholar 

  • Perryman, K.M., Lindsley, D.F., Lindsley, D.B.: Pulvinar unit responses associated with eye movements in squirrel monkeys. Soc. Neurosci. Abstr. 2, 280 (1976)

    Google Scholar 

  • Rakic, P., Sidman, R.L.: Telencephalic origin of pulvinar neurons in the fetal human brain. Z. Anat. Entwickl.-Gesch. 129, 53–82 (1969)

    Google Scholar 

  • Rezak, M., Benevento, L.A.: Topographical organization of extrageniculate thalamic projections to striate cortex and prestriate cortex in the macaque monkey. Soc. Neurosci. Abstr. 2, 1088 (1976) (and in preparation)

    Google Scholar 

  • Rezak, M., Benevento, L.A.: A redefinition of pulvinar subdivisions in the macaque monkey: Evidence for three distinct subregions within classically defined lateral pulvinar. Soc. Neurosci. Abstr. 3, 574 (1977)

    Google Scholar 

  • Rezak, M., Benevento, L.A.: Organization of pulvinar projections to striate cortex (Area 17) in the macaque monkey: Autoradiographic evidence for a specialized subregion of the lateral pulvinar. Anat. Rec. 187, 777 (1977a)

    Google Scholar 

  • Schiller, P.H.: The role of the monkey superior colliculus in eye movement and vision. Invest. Ophthal. 11, 451–460 (1972)

    Google Scholar 

  • Spatz, W.B., Erdmann, G.: Striate cortex projections to the lateral geniculate and other thalamic nuclei; a study using degeneration and autoradiographic tracing methods in the marmoset callitrix. Brain Res. 82, 91–108 (1974)

    Google Scholar 

  • Spatz, W.B., Tigges, J.: Studies on the visual area MT in primates. II. Projection fibers to subcortical structures. Brain Res. 61, 374–378 (1973)

    Google Scholar 

  • Talbot, S.A., Marshall, W.H.: Physiological studies of neural mechanisms of visual localization and discrimination. Amer. J. Ophthal. 24, 1255–1264 (1941)

    Google Scholar 

  • Tigges, J., Spatz, W.B., Tigges, M.: Reciprocal point to point connections between parastriate and striate cortex in the squirrel monkey. J. comp. Neurol. 148, 481–489 (1973)

    Google Scholar 

  • Trojanowski, J., Jacobson, S.: Areal and laminar distribution of some pulvinar cortical efferents in rhesus monkey. J. comp. Neurol. 169, 371–392 (1976)

    Google Scholar 

  • Updyke, B.V.: Retinotopic organization in the pulvinar and lateral posterior nucleus of the cat. Anat. Rec. 184, 552 (1976)

    Google Scholar 

  • Wiesel, T.N., Hubel, D.H., Lam, D.N.K.: Autoradiographic demonstration of ocular-dominance columns in the monkey striate cortex by means of transneuronal transport. Brain Res. 79, 273–279 (1974)

    Google Scholar 

  • Yin, T.C.T., Lynch, J.C., Talbot, W.H., Mountcastle, V.B.: Neuronal mechanisms of parietal lobe for directed visual attention, studied in waking monkeys. Soc. Neurosci. Abstr. 5, 59 (1975)

    Google Scholar 

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

    Google Scholar 

  • Zeki, S.M.: Representation of central visual fields in prestriate cortex of monkey. Brain Res. 14, 271–291 (1969a)

    Google Scholar 

  • Zeki, S.M., Handeman, D.: Combined anatomical and electrophysiological studies on the boundary between the second and third visual areas of rhesus monkey cortex. Proc. Roy. Soc. B 194, 555–562 (1976)

    Google Scholar 

  • Zeki, S.M.: Simultaneous anatomical demonstration of the representation of the vertical and horizontal meridians in areas V2 and V3 of rhesus monkey visual cortex. Proc. Roy. Soc. B 195, 517–523 (1977)

    Google Scholar 

Download references

Author information

Affiliations

  1. College of Medicine, University of Illinois Medical Center, P.O. Box 6998, 60680, Chicago, Illinois, USA

    L. A. Benevento & B. Davis

Authors
  1. L. A. Benevento
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. B. Davis
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

This work was supported by NSF Grant 75-07349. The technical assistance of Mr. Henry Kulikowski is gratefully acknowledged. We are indebted to Drs. M. Rowe and M. Rezak for their comments on the manuscript

B. Davis was supported by a University of Illinois assistantship

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Benevento, L.A., Davis, B. Topographical projections of the prestriate cortex to the pulvinar nuclei in the macaque monkey: An autoradiographic study. Exp Brain Res 30, 405–424 (1977). https://doi.org/10.1007/BF00237265

Download citation

  • Received:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00237265

Key words

  • Inferior pulvinar
  • Adjacent lateral pulvinar
  • Topographical
  • Visual hemifield
  • Cortico-thalamocortical connections