Experimental Brain Research

, Volume 80, Issue 3, pp 532–544 | Cite as

Projections from the medial agranular cortex to brain stem visuomotor centers in rats

  • S. L. Stuesse
  • D. B. Newman
Article

Summary

Projections from medial agranular cortex to brain stem in rat were determined by use of the anterograde tracers Phaseolus vulgaris leucoagglutinin, or wheat germ agglutinin conjugated horseradish peroxidase. Axonal trajectories were also followed by means of the Wiitanen modification of the Fink-Heimer degeneration technique. AGm was identified on the basis of its cytoarchitectonics. AGm projected to the anterior pretectal nucleus, the rostral interstitial nucleus of the medial longitudinal fasciculus, the medial accessory oculomotor nucleus of Bechterew, the interstitial nucleus of Cajal, the nucleus of Darkschewitsch, the nucleus cuneiformis and subcuneiformis, intermediate and deep superior collicular layers, the paramedian pontine reticular formation (reticularis pontis oralis and caudalis, and reticularis gigantocellularis), and raphe centralis superior. Differences in connections between rostral and caudal injections were observed: pontine and medullary projections were lighter from the rostral portion of AGm than from the more caudal portions of AGm. The heaviest projections to the anterior pretectal nucleus were from the caudal portion of AGm. The subcortical projections were very similar to those described for the frontal eye field in monkeys, and the majority of them targeted areas thought to be involved in coordination of gaze with head and neck movements. Thus AGm in rats may contain the homologue of the primate frontal eye fields.

Key words

Frontal cortex Frontal eye fields Reticular formation Brain stem Preoculomotor nuclei Rat 

Abbreviations

3

main oculomotor nucleus

7

facial motor nucleus;

I, II–IV, V, and VI

cortical layers

III

third ventricle

7n

facial nerve

AC

Anterior commissure

AGm

medial agranular cortex

Bec

Nucleus of Bechterew

cc

corpus callosum

Dark

Nucleus of Darkschewitsch

Dc

dorsal cochlear nucleus

DLG

dorsal lateral geniculate nucleus

F

fornix

fr

fasciculus retroflexus

ic

inferior colliculus

Me5

mesencephalic trigeminal nucleus

ml

medial lemniscus

mlf

medial longitudinal fasciculus

Mo5

trigeminal motor nucleus

nV

trigeminal nerve

pc

posterior commissure

pn

pons

Po

posterior thalamic nucleus

PPo

pedunculo-pontine nucleus

PPRF

paramedian pontine reticular formation

py

pyramidal tract

R

red nucleus

RaCs

raphe centralis superior

RaD

dorsal raphe nucleus

RCf

reticularis cuneiformis

RiMLF

rostral interstitial nucleus of the medial longitudinal fasciculus

RMc

reticularis magnocellularis

RPc

reticularis parvocellularis

RPoCa

reticularis pontis caudalis pars alpha

RPoCb

reticularis pontis caudalis pars beta

RPoO

reticularis pontis oralis

RPoOm

reticularis pontis oralis pars medialis

RScf

reticularis subcuneiformis

sc

superior colliculus

SCP

superior cerebellar peduncle

so

superior olive

Sp5

spinal trigeminal nucleus

Tz

trapezoid nucleus

WGA-HRP

wheat germ agglutinin- horseradish peroxidase

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References

  1. Astruc J (1971) Corticofugal connections of area 8 (frontal eye field) in Macaca mulatta. Brain Res 33:241–256Google Scholar
  2. Beckstead RM (1979) An autoradiographic examination of corticocortical and subcortical projections of the medio-dorsal projection (prefrontal) cortex in the rat. J Comp Neurol 184:43–62Google Scholar
  3. Brodal A (1981) Neurological anatomy in relation to clinical medicine. Oxford University Press, New York, pp 485–541, 551–553Google Scholar
  4. Bruce CJ, Goldberg ME (1985) Primate frontal eye fields. I. Single neurons discharging before saccades. J Neurophysiol 53:603–635Google Scholar
  5. Bruce CJ, Goldberg ME, Bushnell C, Stanton GB (1985) Primate frontal eye fields. II. Physiological and anatomical correlates of electrically evoked eye movements. J Neurophysiol 54:715–734Google Scholar
  6. Büttner-Ennever J, Büttner U (1978) A cell group associated with vertical eye movements in the rostral mesencephalic reticular formation of the monkey. Brain Res 151:31–47Google Scholar
  7. Büttner-Ennever J, Cohen F, Pause M, Fries W (1988) Raphe nucleus of the pons containing omnipause neurons of the oculomotor system in the monkey and its homologue in man. J Comp Neurol 267:307–321PubMedGoogle Scholar
  8. Büttner-Ennever J, Holstege G (1986) Anatomy of premotor centers in the reticular formation controlling oculomotor, skeletomotor and autonomic motor system. Prog Brain Res 64:89–98Google Scholar
  9. Cohen B, Komatsuzaki A (1968) Electrooculographic syndrome in monkeys after pontine reticular formation lesions. Arch Neurol 18:78–92Google Scholar
  10. Cohen B, Komatsuzaki A (1972) Eye movements induced by stimulation of the pontine reticular formation: evidence for integration in oculomotor pathways. Exp Neurol 36:101–117Google Scholar
  11. Cohen B, Waitzman DM, Büttner-Ennever JA, Matsuo V (1986) Horizontal saccades and the central mesencephalic reticular formation. Prog Brain Res 64:243–256Google Scholar
  12. Crowne DP (1983) The frontal eye field and attention. Psychol Bull 93:232–260Google Scholar
  13. Donoghue JF, Wise SP (1982) The motor cortex of the rat: cytoarchitecture and microstimulation mapping. J Comp Neurol 212:76–88Google Scholar
  14. Fink RP, Heimer L (1967) Two methods for selective silver impregnation of degenerating axons and their synaptic endings in the central nervous system. Brain Res 4:369–374Google Scholar
  15. Fukushima K (1987) The interstitial nucleus of Cajal and its role in the control of movements of head and eyes. Prog Neurobiol 29:107–192CrossRefPubMedGoogle Scholar
  16. Fuller JH (1985) Eye and head movements in the pigmented rat. Vision Res 25:1121–1128Google Scholar
  17. Gerfen CR, Sawchenko PE (1984) An anterograde neuroanatomical tracing method that shows the detailed morphology of neurons, their axons, and terminals: immunohistochemical localization of an axonally transported plant lectin, Phaseolus vulgaris leucoagglutinin (PHA-L). Brain Res 29:219–238Google Scholar
  18. Gibson AR, Hansma DI, Houk JC, Robinson FR (1984) A sensitive low artifact TMB procedure for the demonstration of WGA-HRP in the CNS. Brain Res 298:235–241Google Scholar
  19. Goldberg ME, Bruce CJ (1986) The role of the arcuate frontal eye fields in the generation of saccadic eye movements. Prog Brain Res 64:143–154Google Scholar
  20. Hall RD, Lindholm EP (1974) Organization of motor and somatosensory neocortex in the albino rat. Brain Res 66:23–38Google Scholar
  21. Hikosaka O, Kawakami T (1977) Inhibitory neurons related to the quick phase of vestibular nystagmus: their location and projection. Exp Brain Res 27:377–396Google Scholar
  22. Hikosaka O, Sakamoto M (1987) Dynamic characteristics of saccadic eye movements in the albino rat. Neurosci Res 4:304–308Google Scholar
  23. Huerta MF, Krubitzer LA, Kass JH (1986) Frontal eye field as defined by intracortical microstimulation in squirrel monkeys, owl monkeys, and macaque monkeys I. Subcortical connections. J Comp Neurol 253:415–439Google Scholar
  24. Kolb B (1984) Functions of the frontal cortex of the rat: a comparative review. Brain Res Rev 8:65–98CrossRefGoogle Scholar
  25. Künzle H, Akert K (1977) Efferent connections of cortical area 8 (frontal eye field) in Macaco fascicularis: a reinvestigation using the autoradiographic technique. J Comp Neurol 173:147–164Google Scholar
  26. Langer TP, Kaneko CRS (1983) Efferent projections of the cat oculomotor reticular omnipause neuron region: an autoradiographic study. J Comp Neurol 217:288–306Google Scholar
  27. Leichnetz GR (1981) The prefrontal cortico-oculomotor trajectories in the monkey. J Neurol Sci 49:387–396Google Scholar
  28. Leichnetz GR (1985) The frontal eye field projects to the nucleus prepositus hypoglossi in the monkey. Neurosci Lett 54:185–188Google Scholar
  29. Leichnetz GR, Gonzalo-Ruiz A (1987) Collateralization of frontal eye field (medial precentral/anterior cingulate) neurons projecting to the paraoculomotor region, superior colliculus, and medial pontine reticular formation in the rat: a fluorescent double-labeling study. Exp Brain Res 68:355–364Google Scholar
  30. Leichnetz GR, Hardy SGP, Carruth MK (1987) Frontal projections to the region of the oculomotor complex in the rat: a retrograde and anterograde HRP study. J Comp Neurol 263:387–399Google Scholar
  31. Leichnetz GR, Smith DJ, Spencer RF (1984a) Cortical projections to the paramedian tegmental and basilar pons in the monkey. J Comp Neurol 228:388–408Google Scholar
  32. Leichnetz GR, Spencer RF, Smith DJ (1984b) Cortical projections to nuclei adjacent to the oculomotor complex in the medial dien-mesencephalic tegmentum in the monkey. J Comp Neurol 228:359–387Google Scholar
  33. Leonard CM (1969) The prefrontal cortex of the rat. I. Cortical projection of the mediodorsal nucleus. II. Efferent connections. Brain Res 12:321–343Google Scholar
  34. Markowitsch HJ, Pritzel M (1977) Comparative analysis of prefrontal learning functions in rats, cats, and monkeys. Psychol Bull 84:817–837Google Scholar
  35. McCrea RA, Baker R, Delgado-Garcia J (1979) Afferent and efferent organization of the prepositus hypoglossi nucleus. Prog Brain Res 50:653–655Google Scholar
  36. McHaffie JG, Stein BE (1982) Eye movements evoked by electrical stimulation in the superior colliculus of rats and hamsters. Brain Res 247:243–253Google Scholar
  37. Mesulam MM (1978) Tetramethyl benzidine for horseradish peroxidase neurochemistry: a noncarcinogenic blue reaction product with superior sensitivity for visualizing neuronal afferents and efferents. J Histochem Cytochem 26:106–117PubMedGoogle Scholar
  38. Mesulam MM (1982) Tracing neural connections with horseradish peroxidase, Chapt 1. John Wiley and Sons, New YorkGoogle Scholar
  39. Mihailoff GA, Lee H, Watt CB, Yates R (1985) Projections to the basilar pontine nuclei from face sensory and motor regions of the cerebral cortex in rat. J Comp Neurol 237:251–263PubMedGoogle Scholar
  40. Neafsey EJ, Bold EL, Haas G, Hurley-Guis KM, Quirk G, Sievert CF, Terreberry RR (1986a) The organization of the rat motor cortex: a micro stimulation mapping study. Brain Res Rev 11:77–96Google Scholar
  41. Neafsey EJ, Hurley-Gius KM, Arvanitis D (1986b) The topographical organization of neurons in the rat medial frontal, insular, and olfactory cortex projecting to the solitary nucleus, olfactory bulb, periaqueductal gray and superior colliculus. Brain Res 377:261–270Google Scholar
  42. Newman DB (1985a) Distinguishing rat brain stem reticulospinal nuclei by their neuronal morphology. I. Medullary nuclei. J Hirnforsch 26:187–226Google Scholar
  43. Newman DB (1985b) Distinguishing brain stem reticulospinal nuclei by their neuronal morphology. II. Pontine and mesencephalic nuclei. J Hirnforsch 26:385–418Google Scholar
  44. Ohgaki T, Curthoys IS, Markham CH (1987) Anatomy of physiologically identified eye movement-related pause neurons in the cat: pontomedullary region. J Comp Neurol 266:56–72Google Scholar
  45. Olszewski J, Baxter D (1954) Cytoarchitecture of the human brain stem. S Karger, New YorkGoogle Scholar
  46. Passingham RE, Myers C, Rawlins N, Lightfoot V, Fearn S (1988) Premotor cortex in the rat. Behav Neurosci 102:101–109Google Scholar
  47. Paxinos G, Watson C (1986) The rat brain in stereotaxic coordinates, 2nd edn. Academic Press, New YorkGoogle Scholar
  48. Peterson BW (1980) Participation of pontomedullary reticular neurons in specific motor activity. In: JA Hobson and MAB Brazier (eds) The reticular formation revisited. Raven Press, pp 171–192Google Scholar
  49. Reep RL (1984) Relationship between prefrontal and limbic cortex: a comparative anatomical review. Brain Behav Evol 25:5–80Google Scholar
  50. Reep RL, Corwin JL, Hashimoto A, Watson RT (1987) Efferent connections of the rostral portion of medial agranular cortex in rats. Brain Res Bull 19:203–221Google Scholar
  51. 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 Res 329:151–160Google Scholar
  52. Schlag J, Schlag-Rey M (1987) Evidence for a supplementary eye field. J Neurophysiol 57:179–200Google Scholar
  53. Sefton AJ, Dreher B (1985) Visual system. In: Paxinos G (ed) The rat nervous system, Vol I. Forebrain and midbrain. Academic Press, New York, pp 169–221Google Scholar
  54. Shook BL, Schlag-Rey M, Schlag J (1988) Direct projections from the supplementary eye field to the nucleus raphe interpositus. Exp Brain Res 73:215–218Google Scholar
  55. Siegel JM, Tomaszewski KS (1983) Behavioral organization of reticular formation: studies in the unrestrained cat. I. Cells related to axial, limb, eye and other movements. J Neurophysiol 50:696–716Google Scholar
  56. Stanton GB, Goldberg ME, Bruce CJ (1988) Frontal eye field efferents in the macaque monkey. II. Topography of terminal fields in midbrain and pons. J Comp Neurol 271:493–506Google Scholar
  57. Strassman A, Highstein SM, McCrea RA (1986a) Anatomy and physiology of saccadic burst neurons in the alert squirrel monkey. I. Excitatory burst neurons. J Comp Neurol 249:337–357PubMedGoogle Scholar
  58. Strassman A, Highstein SM, McCrea RA (1986b) Anatomy and physiology of saccadic burst neurons in the alert squirrel monkey. II. Inhibitory burst neurons J Comp Neurol 249:358–380PubMedGoogle Scholar
  59. Sukekawa K (1988) Reciprocal connections between medial prefrontal cortex and lateral posterior nucleus in rats. Brain Behav Evol 32:246–251Google Scholar
  60. Wiesendanger R, Wiesendanger M (1982b) The corticopontine system in the rat. II. The projection pattern. J Comp Neurol 208:227–238Google Scholar
  61. Wiitanen JT (1969) Selective silver impregnation of degenerating axons and terminals in the central nervous system of the monkey (Macaca mulatta). Brain Res 14:546–548Google Scholar
  62. Wise SP, Donoghue JP (1986) Motor cortex of rodents. In: Jones, EG Peters, A (eds) Cerebral cortex, sensory-motor areas and aspects of cortical connectivity, Vol. 5. Plenum Press, New York, pp 243–270Google Scholar
  63. Zilles K (1985) The cortex of the rat: a stereotaxic atlas. Spinger, BerlinGoogle Scholar
  64. Zilles K, Wree A (1985) Cortex: areal and laminar structure. In: Paxinos G (ed) The rat nervous system. Academic Press, New York, pp 375–416Google Scholar

Copyright information

© Springer-Verlag 1990

Authors and Affiliations

  • S. L. Stuesse
    • 1
  • D. B. Newman
    • 2
  1. 1.Neurobiology DepartmentN.E.Ohio Universities, College of MedicineRootstownUSA
  2. 2.Department of AnatomyF. Hebert School of Medicine, Uniformed Services, University of the Health SciencesBethesdaUSA

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