Frontal eye field projection to the paramedian pontine reticular formation traced with wheat germ agglutinin in the monkey

Injections of the retrograde tracer [125I]wheat germ agglutinin have been placed in different areas of the paramedian pontine reticular formation (PPRF), a well known premotor center for gaze control. Experiments in 5 monkeys revealed 3 major sources of input: (1) bilateral projections from the so-called frontal eye field (FEF), which is situated in the frontal cortex around the arcuate sulcus; (2) the intermediate and deep layers of mainly the contralateral superior colliculus; and (3) ipsilateral projections from brainstem structures such as the accessory oculomotor nuclei (nucleus interstitialis of Cajal, nucleus of Darkschewitsch, and nucleus of the posterior commissure), the mesencephalic reticular formation, the vestibular nuclei, the nucleus prepositus hypoglossi, and the cerebellar fastigial nucleus. The results are compared with previous anatomical investigations and confirm the electrophysiologically demonstrated FEF-PPRF-abducens disynaptic pathway.

[1]  J. L. Conway,et al.  Deficits in eye movements following frontal eye-field and superior colliculus ablations. , 1980, Journal of neurophysiology.

[2]  G. Leichnetz,et al.  The prefrontal cortico-oculomotor trajectories in the monkey A possible explanation for the effects of stimulation/lesion experiments on eye movement , 1981, Journal of the Neurological Sciences.

[3]  David A. Hopkins,et al.  Substantia nigra projections to the reticular formation, superior colliculus and central gray in the rat, cat and monkey , 1976, Neuroscience Letters.

[4]  R. Wurtz,et al.  Enhancement of visual responses in monkey striate cortex and frontal eye fields. , 1976, Journal of neurophysiology.

[5]  J Schlag,et al.  Relations between thalamic and corticofrontal sites of oculomotor control in the cat. , 1973, Brain research.

[6]  L. C. Skeen,et al.  Brainstem projections to the frontal eye field in cat , 1982, Brain Research.

[7]  D. Pfaff,et al.  Efferents from medial basal forebrain and hypothalamus in the rat. II. An autoradiographic study of the anterior hypothalamus , 2004, The Journal of comparative neurology.

[8]  A M Graybiel,et al.  Direct and indirect preoculomotor pathways of the brainstem: An autoradiographic study of the pontine reticular formation in the cat , 1977, The Journal of comparative neurology.

[9]  V. Henn.  Loss of vertical rapid eye movements after kainic acid lesions in the rostral mesencephalon in the rhesus monkey , 1983 .

[10]  B. Cohen,et al.  Unit activity in the pontine reticular formation associated with eye movements , 1972 .

[11]  V. Mountcastle,et al.  Parietal lobe mechanisms for directed visual attention. , 1977, Journal of neurophysiology.

[12]  R. L. McBride,et al.  Amygdaloid and pontine projections to the ventromedial nucleus of the hypothalamus , 1977, The Journal of comparative neurology.

[13]  J. Büttner-Ennever,et al.  A cell group associated with vertical eye movements in the rostral mesencephalic reticular formation of the monkey , 1978, Brain Research.

[14]  M. B. Bender,et al.  Lesions of the pontine tegmentum and conjugate gaze paralysis. , 1971, Archives of neurology.

[15]  P. Brodal,et al.  The corticopontine projection in the rhesus monkey. Origin and principles of organization. , 1978, Brain : a journal of neurology.

[16]  W. W. Kaelber,et al.  Efferent fiber connections of the dorsal and deep tegmental nuclei of Gudden. An experimental study in the cat. , 1971, Brain research.

[17]  O. Pompeiano,et al.  Fastigioreticular fibers in the cat. An experimental study with silver methods , 1962, The Journal of comparative neurology.

[18]  D L Robinson,et al.  Behavioral enhancement of visual responses of prestriate neurons of the rhesus monkey. , 1980, Investigative ophthalmology & visual science.

[19]  C. K. Henkel,et al.  Superior colliculus connections with the extraocular motor nuclei in the cat , 1978, The Journal of comparative neurology.

[20]  J. Büttner-Ennever,et al.  An autoradiographic study of the pathways from the pontine reticular formation involved in horizontal eye movements , 1976, Brain Research.

[21]  Y. Agid,et al.  Labeled wheat germ agglutinin (WGA) as a new, highly sensitive retrograde tracer in the rat brain hippocampal system , 1978, Brain Research.

[22]  Ray S. Snider,et al.  A stereotaxic atlas of the monkey brain : (Macaca mulatta) , 1961 .

[23]  G. Leichnetz.  The medial accessory nucleus of bechterew: A cell group within the anatomical limits of the rostral oculomotor complex receives a direct prefrontal projection in the monkey , 1982, The Journal of comparative neurology.

[24]  H. Thoenen,et al.  Role of gangliosides in the uptake and retrograde axonal transport of cholera and tetanus toxin as compared to nerve growth factor and wheat germ agglutinin , 1977, Brain Research.

[25]  J. Büttner-Ennever,et al.  Oculomotor nucleus afferents in the monkey demonstrated with horseradish peroxidase , 1979, Brain Research.

[26]  K. Akert,et al.  Efferent connections of cortical, area 8 (frontal eye field) in Macaca fascicularis. A reinvestigation using the autoradiographic technique , 1977, The Journal of comparative neurology.

[27]  C. Galletti,et al.  Cortico-cortical connections from the visual region of the superior tempora sulcus to frontal eye field in the macaque , 1983, Brain Research.

[28]  E. Keller.  Participation of medial pontine reticular formation in eye movement generation in monkey. , 1974, Journal of neurophysiology.

[29]  A. Gibson,et al.  Visual cells in the pontine nuclei of the cat. , 1976, The Journal of physiology.

[30]  K. Akert,et al.  Cortical area 8 and its thalamic projection in Macaca mulatta , 1963, The Journal of comparative neurology.

[31]  A. Brodal,et al.  Experimental studies of commissural and reticular formation projections from the vestibular nuclei in the cat. , 1968, Brain research.

[32]  K. Akert,et al.  A comparison of the retrograde tracer properties of [125I] wheat germ agglutinin (WGA) with HRP after injection into the corpus callosum , 1982, Brain Research.

[33]  A. Fuchs,et al.  Activity of brain stem neurons during eye movements of alert monkeys. , 1972, Journal of neurophysiology.

[34]  J. K. Harting.  Descending pathways from the superior colliculus: An autoradiographic analysis in the rhesus monkey (Macaca mulatta) , 1977, The Journal of comparative neurology.

[35]  W. Cowan,et al.  The efferent connections of the ventromedial nucleus of the hypothalamus of the rat , , 1976, The Journal of comparative neurology.

[36]  Ruth Bleier,et al.  A Stereotaxic Atlas of the Monkey Brain (Macaca mulatta).by Ray S. Snider; John C. Lee;A Stereotaxic Atlas of the Cat Brain.by Ray S. Snider; William T. Niemer , 1963 .

[37]  J. Graham.  An autoradiographic study of the efferent connections of the superior colliculus in the cat , 1977, The Journal of comparative neurology.

[38]  G. Bonin,et al.  The neocortex of Macaca mulatta , 1947 .

[39]  G. B. Stanton.  Afferents to oculomotor nuclei from area “y” in Macaca mulatta: An anterograde degeneration study , 1980, The Journal of comparative neurology.

[40]  J. E. Albano,et al.  Visual-motor function of the primate superior colliculus. , 1980, Annual review of neuroscience.

[41]  J. Büttner-Ennever.  Organization of reticular projections onto oculomotor neurones. , 1979, Progress in brain research.

[42]  M B Carpenter,et al.  Fastigial efferent projections in the monkey: An autoradiographic study , 1977, The Journal of comparative neurology.

[43]  K Hepp,et al.  The primate oculomotor system. I. Motoneurons. A synthesis of anatomical, physiological, and clinical data. , 1982, Human neurobiology.

[44]  W. Mehler,et al.  Physiology and anatomy of the cortico-oculomotor mechanism. , 1972, Progress in brain research.

[45]  Mortimer Mishkin,et al.  Mapping the primate visual system with [2-14C]deoxyglucose. , 1982, Science.