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Preoccipital cortex receives a differential input from the frontal eye field and projects to the pretectal olivary nucleus and other visuomotor-related structures in the rhesus monkey

Published online by Cambridge University Press:  02 June 2009

G. R. Leichnetz
G. R. Leichnetz
Affiliation:
Department of Anatomy, Medical College of Virginia, Virginia Commonwealth University, Richmond
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Abstract

The bidirectional axonal transport capabilities of the horseradish peroxidase (HRP) technique facilitated the study of the frontal-eye-field (FEF) input and pretectal output of two regions of extrastriate preoccipital cortex (POC). Following horseradish peroxidase (HRP) gel implants into the middle and dorsal POC in two rhesus monkeys, the middle POC implant demonstrated retrograde frontal cortical labeling largely restricted to the inferior frontal eye field (iFEF) and adjacent inferior prefrontal convexity, whereas the dorsal POC implant showed labeling in the caudal ventral bank of the superior ramus of the arcuate sulcus (sas) and middle-to-dorsal region of the rostral bank of the concavity of the arcuate sulcus (dorsal FEF). Prominent anterogradely labeled efferent preoccipital projections were observed to the ipsilateral pretectal olivary nucleus (PON) and to a lesser extent the anterior pretectal nucleus. Although the middle POC case had heavier projections to the lateral PON, the dorsal case projected more heavily to the medial PON. In addition, both implants demonstrated subcortical connections with the lateral and dorsal inferior pulvinar nuclei, central superior lateral thalamic intralaminar nucleus, caudate nucleus, and middle-to-ventral claustrum. However, while the middle POC implant had efferent projections to the superficial superior colliculus (SC), pregeniculate nucleus (PGN), lateral terminal accessory optic nucleus (LTN), and dorsolateral pontine nucleus (DLPN), resembling those previously reported for the middle temporal (MT) visual area (Maunsell & Van Essen, 1982; Ungerleider et al., 1984), the dorsal implant had projections to the lateral intermediate SC, zona incerta (ZI), PGN, a notably lesser projection to the LTN, and basilar pontine projections to the lateral and lateral dorsal pontine subnuclei (not including the extreme dorsolateral DLPN).

These preliminary results suggest that the preoccipital cortex, which reportedly functions in pupillary constriction, accommodation, and convergence, entertains connections with the PON and other visuomotorrelated structures, and thus could act as an intermediary in the pathway between the iFEF and PON, and provide a possible explanation for pupillary effects that occur with stimulation of the FEF (Jampel, 1960) and within the context of other oculomotor activities. The findings shed light on certain differences in connections of middle vs. dorsal POC with visuomotor-related nuclei, and appear to suggest that the middle region, which receives input from the iFEF, has greater access to the optokinetic (OKN) system by virtue of its projection to the LTN, and to the smooth-pursuit system by virtue of its projection to the DLPN.

Keywords

Prelunate gyrusSuperior temporal sulcal cortexMiddle temporal areaMedial superior temporal areaSuperior colliculusLateral terminal accessory optic nucleusDorsolateral basilar pontine nucleusZona incertaPregeniculate nucleusSaccadic eye movementsSmooth-pursuit eye movementsPupillary constriction
Type
Research Article
Information
Visual Neuroscience , Volume 5 , Issue 2 , August 1990 , pp. 123 - 133
Copyright
Copyright © Cambridge University Press 1990

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References

Asanuma, C., Anderson, R.A. & Cowan, W. M. (1985). The thalamic relations of the caudal inferior parietal lobule and the lateral prefrontal cortex in monkeys: divergent cortical projections from cell clusters in the medial pulvinar nucleus. Journal of Comparative Neurology 241, 357–381.CrossRefGoogle ScholarPubMed
Barbas, H. & Mesulam, M.-M. (1981). Organization of afferent input to subdivisions of area 8 in the rhesus monkey. Journal of Comparative Neurology 200, 407–431.CrossRefGoogle ScholarPubMed
Benevento, L.A. & Davis, B. (1977). Topographical projections of the prestriate cortex to the pulvinar nuclei in the macaque monkey: an autoradiographic study. Experimental Brain Research 30, 405–424.Google Scholar
Benevento, L.A., Rezak, M. & Santos-Anderson, R. (1977). An autoradiographic study of the projections of the pretectum in the rhesus monkeys (Macaca mulatta): evidence for sensorimotor links to the thalamus and oculomotor nuclei. Brain Research 127, 197–218.CrossRefGoogle Scholar
Bruce, C.J., Goldberg, M.E., Bushnell, M.C. & Stanton, G.B. (1985). Primate frontal eye fields, II. Physiological and anatomical correlatives of electrically evoked eye movements. Journal of Neurophysiology 54, 714–734.CrossRefGoogle ScholarPubMed
Burde, R.M. & Loewy, A.D. (1980). Central origin of oculomotor parasympathetic neurons in the monkey. Brain Research 198, 434–439.CrossRefGoogle ScholarPubMed
Carpenter, M.B. & Pierson, R.J. (1973). Pretectal region and the pupillary light reflex: an anatomical analysis in the monkey. Journal of Comparative Neurology 149, 271–300.CrossRefGoogle ScholarPubMed
Clarke, R.J. & Ikeda, H. (1981). Pupillary response and luminance-and darkness-detector neurones in the pretectum of the rat. Documenta Ophthalmologia, The Hague, Series 30, pp. 53–61.Google Scholar
Clarke, R.J. & Ikeda, H. (1985). Luminance and darkness detectors in the olivary and posterior pretectal nuclei and their relationship to the pupillary light reflex in the rat, I: Studies with steady luminance levels. Experimental Brain Research 57, 224–232.CrossRefGoogle Scholar
Dineen, J.T. & Hendrickson, A. (1983). Overlap of retinal and prestriate cortical pathways in the primate pretectum. Brain Research 278, 250–254.Google ScholarPubMed
Distler, C. & Hoffmann, K.-P. (1989 a). The pupillary light reflex in normal and innate microstrabismic cats, I: Behavior and receptive-field analysis in the nucleus praetectalis olivaris. Visual Neuroscience 3, 127–138.CrossRefGoogle ScholarPubMed
Distler, C. & Hoffmann, K.-P. (1989 b). The pupillary light reflex in normal and innate microstrabismic cats, II: Retinal and cortical input to the nucleus praetectalis olivaris. Visual Neuroscience 3, 139–153.CrossRefGoogle Scholar
Dürsteler, M.R. & Wurtz, R.H. (1988). Pursuit and optokinetic deficits following chemical lesions of cortical areas MT and MST. Journal of Neurophysiology 60, 940–965.CrossRefGoogle ScholarPubMed
Dürsteler, M.R.Wurtz, R.H. & Newsome, W.T. (1987). Directional-pursuit deficits following lesions of the foveal representation within the superior temporal sulcus of the macaque monkey. Journal of Neurophysiology 57, 1262–1287.CrossRefGoogle ScholarPubMed
Edwards, S.B., Ginsburgh, C.I., Henkel, C.K. & Stein, B.E. (1979). Sources of subcortical projections to the superior colliculus in the cat. Journal of Comparative Neurology 184, 309–330.CrossRefGoogle Scholar
Ferrier, D. (1876). The Functions of the Brain. New York: G.P. Putnam.CrossRefGoogle Scholar
Giolli, R.A., Torigoe, Y. & Blanks, R.H. (1988). Non-retinal projections to the medial terminal accessory optic nucleus in the rabbit and rat: a retrograde and anterograde transport study. Journal of Comparative Neurology 269, 73–86.CrossRefGoogle Scholar
Gonzalo-Ruiz, A., Leichnetz, G.R. & Smith, D.J. (1988). Origin of cerebellar projections to the region of the oculomotor complex, medial pontine reticular formation, and superior colliculus in New World monkeys: a retrograde horseradish peroxidase study. Journal of Comparative Neurology 268, 508–526.CrossRefGoogle Scholar
Grofova, I., Ottersen, O.P. & Rinvik, E. (1978). Mesencephalic and diencephalic afferents to the superior colliculus and periaqueductal gray substance demonstrated by retrograde axonal transport of horseradish peroxidase in the cat. Brain Research 146, 205–220.CrossRefGoogle Scholar
Huerta, M.F., Krubitzer, L.A. & Kaas, J.H. (1986). Frontal eye field as defined by intracortical microstimulation in squirrel monkeys, owl monkeys, and macaque monkeys, I: Subcortical connections. Journal of Comparative Neurology 253, 415–442.CrossRefGoogle ScholarPubMed
Hutchins, B. & Weber, J.T. (1980). The pretectal complex of the monkey: a reinvestigation of the morphology and retinal terminations. Journal of Comparative Neurology 232, 425–442.CrossRefGoogle Scholar
Jampel, R.S. (1960). Convergence, divergence, pupillary reactions, and accommodations of the eye from faradic stimulation of the macaque brain. Journal of Comparative Neurology 115, 371–399.CrossRefGoogle ScholarPubMed
Keating, E.G., Gooley, S.G., Pratt, S.E. & Kelsey, J.E. (1983). Removing the superior colliculus silences eye movements normally evoked from stimulation of the parietal and occipital eye fields. Brain Research 269, 191–210.CrossRefGoogle ScholarPubMed
Komatsu, H. & Wurtz, R.H. (1988). Relation of cortical areas MT and MST to pursuit eye movements. Journal of Neurophysiology 60, 580–603.CrossRefGoogle ScholarPubMed
Komatsu, H. & Wurtz, R.H. (1989). Modulation of pursuit eye movements by stimulation of cortical areas MT and MST. Journal of Neurophysiology 62, 31–47.CrossRefGoogle ScholarPubMed
Künzle, H. & Akert, K. (1977). Efferent connections of cortical area 8 (frontal eye field) in Macaca fascicularis. A reinvestigation using the autoradiographic technique. Journal of Comparative Neurology 235, 1–25.Google Scholar
Leichnetz, G.R. (1982). Connections between the frontal eye field and pretectum in the monkey: an anterograde/retrograde study using HRP gel and TMB neurohistochemistry. Journal of Comparative Neurology 207, 394–402.CrossRefGoogle ScholarPubMed
Leichnetz, G.R. (1989). Inferior frontal eye-field projections to the middle temporal (MT) visual area and pursuit-related dorsolateral pontine nucleus in the monkey. Visual Neuroscience 3, 171–180.CrossRefGoogle Scholar
Leichnetz, G.R. & Goldberg, M.E. (1988). Higher centers concerned with eye movement and visual attention: cerebral cortex and thalamus. In Neuroanatomy of the Oculomotor System, ed. Buttner-Ennever, J.A., pp. 365–429. Amsterdam: Elsevier Biomedical Publishers.Google Scholar
Leichnetz, G.R., Spencer, R.F., Hardy, S.G.P. & Astruc, J.A. (1981). The prefrontal corticotectal projection in the monkey: an anterograde and retrograde horseradish peroxidase study. Neuroscience 6, 1023–1041.CrossRefGoogle ScholarPubMed
Leichnetz, G.R., Spencer, R.F. & Smith, D.J. (1984 a). Cortical projections to nuclei adjacent to the oculomotor complex in the medial dien-mesencephalic tegmentum in the monkey. Journal of Comparative Neurology 228, 359–387.CrossRefGoogle Scholar
Leichnetz, G.R., Smith, D.J. & Spencer, R.F. (1984 b). Cortical projections to the paramedian tegmental and basilar pons in the monkey. Journal of Comparative Neurology 228, 388–408.CrossRefGoogle Scholar
Li, C.-Y., Tanaka, M. & Creutzfeldt, O.D. (1989). Attention and eye-movement-related activation of neurons in the dorsal prelunate gyrus (area DP). Brain Research 496, 307–313.CrossRefGoogle ScholarPubMed
Lynch, J.C. (1987). Frontal eye-field lesions in monkeys disrupt visual pursuit. Experimental Brain Research 68, 437–441.CrossRefGoogle ScholarPubMed
Lynch, J.C. & McLaren, J.W. (1983). Optokinetic nystagmus deficits following parieto-occipital cortex lesions in monkeys. Experimental Brain Research 49, 125–130.CrossRefGoogle ScholarPubMed
Lynch, J.C., Graybiel, A.M. & Lobeck, L.J. (1985). The differential projections of two cytoarchitectonic subregions of the inferior parietal lobule of macaque upon the deep layers of the superior colliculus. Journal of Comparative Neurology 235, 241–254.CrossRefGoogle ScholarPubMed
MacAvoy, M.C., Bruce, C.J. & Gottlieb, J. (1988). Smooth-pursuit eye movements elicited by microstimulation in the frontal eye-field region of alert macaque monkeys. Society for Neuroscience Abstracts 386 (9), 956.Google Scholar
Maguire, W.M. & Baizer, J.S. (1984). Visuotopic organization of the prelunate gyrus in rhesus monkey. Journal of Neuroscience 4, 1690–1704.CrossRefGoogle ScholarPubMed
Maioli, M.G., Squatrito, S. & Domenciconi, R. (1989). Projections from visual cortical areas of the superior temporal sulcus to the lateral terminal nucleus of the accessory optic system in macaque monkeys. Brain Research 498, 389–392.CrossRefGoogle Scholar
Maunsell, J.H.R. & Newsome, W.T. (1987). Visual processing in monkey extrastriate cortex. Annual Review of Neuroscience 10, 363–401.CrossRefGoogle ScholarPubMed
Maunsell, J.H.R. & Van Essen, D.C. (1982). The connections of the middle temporal visual area in the macaque monkey. Society for Neuroscience Abstracts 8, 811.Google Scholar
Maunsell, J.H.R. & Van Essen, D.C. (1983). The connections of the middle temporal visual area (MT) and their relationship to a cortical hierarchy in the macaque monkey. Journal of Neuroscience 3, 2563–2586.CrossRefGoogle ScholarPubMed
May, J.G., Keller, E.L. & Suzuki, D.A. (1988). Smooth-pursuit eye movement deficits with chemical lesions in the dorsolateral pontine nucleus of the monkey. Journal of Neurophysiology 59, 952–975.Google ScholarPubMed
May, P.J. & Hall, W.C. (1986). The cerebellotectal pathway in the grey squirrel. Experimental Brain Research 65, 200–212.CrossRefGoogle ScholarPubMed
Mesulam, M.-M. (1978). A tetramethylbenzidine method for the light-microscopic tracing of neural connections with horseradish peroxidase (HRP) neurohistochemistry. In Neuroanatomical Techniques–Short Course, Bethesda, Maryland: Society for Neuroscience, pp. 65–71.Google Scholar
Mustari, M.J., Fuchs, A.F. & Wallman, J. (1988). Response properties of dorsolateral pontine units during smooth pursuit in the rhesus macaque. Journal of Neurophysiology 60, 664–686.CrossRefGoogle ScholarPubMed
Nakamura, H. & Kawamura, S. (1988). The ventral lateral geniculate nucleus in the cat: thalamic and commissural connections revealed by the use of WGA-HRP transport. Journal of Comparative Neurology 227, 509–528.CrossRefGoogle Scholar
Newsome, W.T., Wurtz, R.H., Dürsteler, M.R. & Mikami, A. (1985). Deficits in visual motion perception following ibotenic acid lesions of the middle temporal visual area of the macaque monkey. Journal of Neuroscience 5, 825–840.Google ScholarPubMed
Precht, W. (1982). Anatomical and functional organization of optokinetic pathways. In Functional Basis of Ocular Motility Disorders, ed. Lennerstrand, G., Zee, D.S. & Keller, E.L., pp. 291–302. Oxford: Pergamon Press.Google Scholar
Rieck, R.W., Huerta, M.F., Harting, J.K. & Weber, J.T. (1986). Hypothalamic and ventral thalamic projections to the superior colliculus in the cat. Journal of Comparative Neurology 243, 249–265.CrossRefGoogle Scholar
Schnyder, H., Reisine, H., Hepp, K. & Henn, V. (1985). Frontal eye-field projection to the paramedian pontine reticular formation traced with wheat germ agglutinin in the monkey. Brain Research 329, 151–160.CrossRefGoogle Scholar
Seltzer, B. & Pandya, D.N. (1978). Afferent cortical connections and architectonics of the superior temporal sulcus and surrounding cortex in the rhesus monkey. Brain Research 149, 1–24.CrossRefGoogle ScholarPubMed
Shibutani, H., Sakata, H. & Hyvärinen, J. (1984). Saccade and blinking evoked by microstimulation of the posterior parietal association cortex of the monkey. Experimental Brain Research 55, 1–8.CrossRefGoogle ScholarPubMed
Stanton, G.B., Goldberg, M.E. & Bruce, C.J. (1988 a). Frontal eye-field efferents in the macaque monkey, I: Subcortical pathways and topography of striatal and thalamic terminal fields. Journal of Comparative Neurology 271, 473–492.CrossRefGoogle ScholarPubMed
Stanton, G.B., Goldberg, M.E. & Bruce, C.J. (1988 b). Frontal eye-field efferents in the macaque monkey, II: Topography of terminal fields in midbrain and pons. Journal of Comparative Neurology 271, 493–506.CrossRefGoogle ScholarPubMed
Steiger, H.-J. & Büttner-Ennever, J.A. (1979). Oculomotor nucleus afferents in the monkey demonstrated with horseradish peroxidase. Brain Research 160, 1–15.CrossRefGoogle ScholarPubMed
Suzuki, D.A., May, J.G. & Keller, E.L. (1984). Smooth-pursuit eye movement deficits with pharmacological lesions in monkey dorsolateral pontine nucleus. Society for Neuroscience 10, 58.Google Scholar
Taylor, A.M. & Lieberman, A.R. (1987). Ultrastructural organization of the projection from the superior colliculus to the ventral lateral geniculate nucleus of the rat. Journal of Comparative Neurology 256, 454–462.CrossRefGoogle Scholar
Thier, R., Koehler, W. & Buettner, U.W. (1988). Neuronal activity in the dorsolateral pontine nucleus of the alert monkey modulated by visual stimuli and eye movements. Experimental Brain Research 70, 496–512.CrossRefGoogle ScholarPubMed
Torigoe, Y., Blanks, R.H. & Precht, W. (1986). Anatomical studies on the nucleus reticularis tegmenti pontis in the pigmented rat, II: Subcortical afferents demonstrated by the retrograde transport of horseradish peroxidase. Journal of Comparative Neurology 243, 88–105.CrossRefGoogle ScholarPubMed
Trejo, L.J. & Cicerone, C.M. (1984). Cells in the pretectal olivary nucleus are in the pathway for the direct light reflex of the pupil in the rat. Brain Research 300, 49–62.CrossRefGoogle ScholarPubMed
Tusa, R.J. & Ungerleider, L.G. (1988). Fiber pathways of cortical areas mediating smooth-pursuit eye movements in monkeys. Annals of Neurology 23, 174–183.CrossRefGoogle ScholarPubMed
Ungerleider, L.G. & Desimone, R. (1986). Cortical connections of visual area MT in the macaque. Journal of Comparative Neurology 248, 190–222.CrossRefGoogle ScholarPubMed
Ungerleider, L.G., Desimone, R., Galkin, T.W. & Mishkin, M. (1984). Subcortical projections of area MT in the macaque. Journal of Comparative Neurology 223, 368–386.CrossRefGoogle ScholarPubMed
Velayos, J.L., Jimenez-Castellanos, J. & Reinosos-Suarez, F. (1989). Topographical organization of the projections from the reticular thalamic nucleus to the intralaminar and medial thalamic nuclei in the cat. Journal of Comparative Neurology 279, 457–469.CrossRefGoogle Scholar
Vertes, R.P. & Martin, G.F. (1988). Autoradiographic analysis of ascending projections from the pontine and mesencephalic reticular formation and the median raphe nucleus in the rat. Journal of Comparative Neurology 275, 511–541.CrossRefGoogle ScholarPubMed
Wagman, I. (1964). Eye movements induced by electrical stimulation of cerebrum in monkeys and their relationship to bodily movements. In The Oculomotor System, pp. 18–39. New York: Harper and Row.Google Scholar
Watts, A.G., Swanson, L.W. & Sanchez-Watts, G. (1987). Efferent projections of the suprachiasmatic nucleus, I: Studies using anterograde transport of the phaseolus vulgaris leucoagglutinin in the rat. Journal of Comparative Neurology 258, 204–229.CrossRefGoogle ScholarPubMed
Yeterian, E.H. & Pandya, D.N. (1989). Thalamic connections of the cortex of the superior temporal sulcus in the rhesus monkey. Journal of Comparative Neurology 282, 80–97.CrossRefGoogle ScholarPubMed
Yukie, M. & Iwai, E. (1981). Direct projection from the dorsal lateral geniculate nucleus to the prestriate cortex in macaque monkeys. Journal of Comparative Neurology 201, 81–97.CrossRefGoogle Scholar
Zeki, S.M. (1974). Functional organization of a visual area in the posterior bank of the superior temporal sulcus of the rhesus monkey. Journal of Physiology 236, 549–573.CrossRefGoogle ScholarPubMed
Zimny, R., Grottel, K. & Kotecki, A. (1986). Evidence for cerebellar afferents to the ventral lateral geniculate nucleus and the lateral terminal nucleus of the accessory optic system in the rabbit. A morphological study with comments on the organizational features of visuo-oculomotor-trunco-cerebellar loops. Journal für Hirnforschung 27, 159–212.Google Scholar