A Central Mesencephalic Reticular Formation Projection to the Supraoculomotor Area in Macaque Monkeys

Overview

Journal Brain Struct Funct

Specialty Neurology

Date 2015 Apr 11

PMID 25859632

Citations 14

Authors

Martin O Bohlen

Susan Warren

Paul J May

Affiliations

Soon will be listed here.

Abstract

The central mesencephalic reticular formation is physiologically implicated in oculomotor function and anatomically interwoven with many parts of the oculomotor system's premotor circuitry. This study in Macaca fascicularis monkeys investigates the pattern of central mesencephalic reticular formation projections to the area in and around the extraocular motor nuclei, with special emphasis on the supraoculomotor area. It also examines the location of the cells responsible for this projection. Injections of biotinylated dextran amine were stereotaxically placed within the central mesencephalic reticular formation to anterogradely label axons and terminals. These revealed bilateral terminal fields in the supraoculomotor area. In addition, dense terminations were found in both the preganglionic Edinger-Westphal nuclei. The dense terminations just dorsal to the oculomotor nucleus overlap with the location of the C-group medial rectus motoneurons projecting to multiply innervated muscle fibers suggesting they may be targeted. Minor terminal fields were observed bilaterally within the borders of the oculomotor and abducens nuclei. Injections including the supraoculomotor area and oculomotor nucleus retrogradely labeled a tight band of neurons crossing the central third of the central mesencephalic reticular formation at all rostrocaudal levels, indicating a subregion of the nucleus provides this projection. Thus, these experiments reveal that a subregion of the central mesencephalic reticular formation may directly project to motoneurons in the oculomotor and abducens nuclei, as well as to preganglionic neurons controlling the tone of intraocular muscles. This pattern of projections suggests an as yet undetermined role in regulating the near triad.

Citing Articles

Brainstem sources of input to the central mesencephalic reticular formation in the macaque.

Warren S, May P Exp Brain Res. 2023; 241(8):2145-2162.

PMID: 37474798 DOI: 10.1007/s00221-023-06641-6.

Superior colliculus projections to target populations in the supraoculomotor area of the macaque monkey.

May P, Bohlen M, Perkins E, Wang N, Warren S Vis Neurosci. 2022; 38.

PMID: 36438664 PMC: 9699455. DOI: 10.1017/s095252382100016x.

Neural control of rapid binocular eye movements: Saccade-vergence burst neurons.

Quinet J, Schultz K, May P, Gamlin P Proc Natl Acad Sci U S A. 2020; 117(46):29123-29132.

PMID: 33139553 PMC: 7682339. DOI: 10.1073/pnas.2015318117.

Is Primate Lens Accommodation Unilaterally or Bilaterally Controlled?.

May P, Gamlin P Invest Ophthalmol Vis Sci. 2020; 61(8):5.

PMID: 32634204 PMC: 7425735. DOI: 10.1167/iovs.61.8.5.

Response Properties of Cells Within the Rostral Superior Colliculus of Strabismic Monkeys.

Upadhyaya S, Das V Invest Ophthalmol Vis Sci. 2019; 60(13):4292-4302.

PMID: 31618766 PMC: 6996666. DOI: 10.1167/iovs.19-27786.

References

Moschovakis A, Karabelas A, Highstein S . Structure-function relationships in the primate superior colliculus. I. Morphological classification of efferent neurons. J Neurophysiol. 1988; 60(1):232-62. DOI: 10.1152/jn.1988.60.1.232. View

Pathmanathan J, Cromer J, Cullen K, Waitzman D . Temporal characteristics of neurons in the central mesencephalic reticular formation of head unrestrained monkeys. Exp Brain Res. 2005; 168(4):471-92. DOI: 10.1007/s00221-005-0105-z. View

Warren S, Waitzman D, May P . Anatomical evidence for interconnections between the central mesencephalic reticular formation and cervical spinal cord in the cat and macaque. Anat Rec (Hoboken). 2008; 291(2):141-60. PMC: 2859179. DOI: 10.1002/ar.20644. View

Grantyn A, Grantyn R . Axonal patterns and sites of termination of cat superior colliculus neurons projecting in the tecto-bulbo-spinal tract. Exp Brain Res. 1982; 46(2):243-56. DOI: 10.1007/BF00237182. View

Erichsen J, May P . The pupillary and ciliary components of the cat Edinger-Westphal nucleus: a transsynaptic transport investigation. Vis Neurosci. 2002; 19(1):15-29. DOI: 10.1017/s0952523801191029. View

Dun S, Brailoiu G, Mizuo K, Yang J, Chang J, Dun N . Neuropeptide B immunoreactivity in the central nervous system of the rat. Brain Res. 2005; 1045(1-2):157-63. DOI: 10.1016/j.brainres.2005.03.024. View

Spencer R, Porter J . Biological organization of the extraocular muscles. Prog Brain Res. 2005; 151:43-80. DOI: 10.1016/S0079-6123(05)51002-1. View

Tanaka H, Yoshida T, Miyamoto N, Motoike T, Kurosu H, Shibata K . Characterization of a family of endogenous neuropeptide ligands for the G protein-coupled receptors GPR7 and GPR8. Proc Natl Acad Sci U S A. 2003; 100(10):6251-6. PMC: 156358. DOI: 10.1073/pnas.0837789100. View

May P, Sun W, Erichsen J . Defining the pupillary component of the perioculomotor preganglionic population within a unitary primate Edinger-Westphal nucleus. Prog Brain Res. 2008; 171:97-106. PMC: 2859175. DOI: 10.1016/S0079-6123(08)00613-4. View

10.

Bachtell R, Tsivkovskaia N, Ryabinin A . Alcohol-induced c-Fos expression in the Edinger-Westphal nucleus: pharmacological and signal transduction mechanisms. J Pharmacol Exp Ther. 2002; 302(2):516-24. DOI: 10.1124/jpet.102.036046. View

11.

Blanks R, Clarke R, Lui F, GIOLLI R, Van Pham S, Torigoe Y . Projections of the lateral terminal accessory optic nucleus of the common marmoset (Callithrix jacchus). J Comp Neurol. 1995; 354(4):511-32. DOI: 10.1002/cne.903540404. View

12.

van Leeuwen A, COLLEWIJN H, Erkelens C . Dynamics of horizontal vergence movements: interaction with horizontal and vertical saccades and relation with monocular preferences. Vision Res. 1999; 38(24):3943-54. DOI: 10.1016/s0042-6989(98)00092-3. View

13.

May P, Reiner A, Ryabinin A . Comparison of the distributions of urocortin-containing and cholinergic neurons in the perioculomotor midbrain of the cat and macaque. J Comp Neurol. 2008; 507(3):1300-16. PMC: 2863095. DOI: 10.1002/cne.21514. View

14.

Pathmanathan J, Presnell R, Cromer J, Cullen K, Waitzman D . Spatial characteristics of neurons in the central mesencephalic reticular formation (cMRF) of head-unrestrained monkeys. Exp Brain Res. 2005; 168(4):455-70. DOI: 10.1007/s00221-005-0104-0. View

15.

Horn A, Eberhorn A, Hartig W, Ardeleanu P, Messoudi A, Buttner-Ennever J . Perioculomotor cell groups in monkey and man defined by their histochemical and functional properties: reappraisal of the Edinger-Westphal nucleus. J Comp Neurol. 2008; 507(3):1317-35. DOI: 10.1002/cne.21598. View

16.

Ugolini G, Klam F, Doldan Dans M, Dubayle D, Brandi A, Buttner-Ennever J . Horizontal eye movement networks in primates as revealed by retrograde transneuronal transfer of rabies virus: differences in monosynaptic input to "slow" and "fast" abducens motoneurons. J Comp Neurol. 2006; 498(6):762-85. DOI: 10.1002/cne.21092. View

17.

Erkelens C, Steinman R, COLLEWIJN H . Ocular vergence under natural conditions. II. Gaze shifts between real targets differing in distance and direction. Proc R Soc Lond B Biol Sci. 1989; 236(1285):441-65. DOI: 10.1098/rspb.1989.0031. View

18.

Waitzman D, Van Horn M, Cullen K . Neuronal evidence for individual eye control in the primate cMRF. Prog Brain Res. 2008; 171:143-50. DOI: 10.1016/S0079-6123(08)00619-5. View

19.

Perkins E, Warren S, May P . The mesencephalic reticular formation as a conduit for primate collicular gaze control: tectal inputs to neurons targeting the spinal cord and medulla. Anat Rec (Hoboken). 2009; 292(8):1162-81. PMC: 2773470. DOI: 10.1002/ar.20935. View

20.

Mays L, Porter J . Neural control of vergence eye movements: activity of abducens and oculomotor neurons. J Neurophysiol. 1984; 52(4):743-61. DOI: 10.1152/jn.1984.52.4.743. View