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.
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Abbreviations
- BC:
-
Brachium conjunctivum
- BDA:
-
Biotinylated dextran amine
- CC:
-
Caudal central subdivision of III
- CG:
-
Central gray
- cMRF:
-
Central mesencephalic reticular formation
- DR:
-
Dorsal raphe
- EWcp:
-
Edinger–Westphal, centrally projecting nucleus
- EWpg:
-
Edinger–Westphal, preganglionic nucleus
- FR:
-
Fasciculus retroflexus
- III:
-
Oculomotor nucleus
- IIIn:
-
Oculomotor nerve
- InC:
-
Interstitial nucleus of Cajal
- LL:
-
Lateral lemniscus
- MD:
-
Mediodorsal thalamic nucleus
- MGN:
-
Medial geniculate nucleus
- MIF:
-
Multiply innervated fibers
- MLF:
-
Medial longitudinal fasciculus
- MRF:
-
Midbrain reticular formation
- nD:
-
Nucleus of Darkschewitsch
- nPC:
-
Nucleus of the posterior commissure
- OPt:
-
Olivary pretectal nucleus
- P:
-
Pyramidal tract
- PAG:
-
Periaqueductal gray
- PC:
-
Posterior commissure
- PhaL:
-
Phaseolus vulgaris leucoagglutinin
- piMRF:
-
Peri-interstitial nucleus of Cajal region of the MRF
- PPRF:
-
Paramedian pontine reticular formation
- PRF:
-
Pontine reticular formation
- Pul:
-
Pulvinar
- RCL:
-
Caudal linear nucleus of the raphe
- RN:
-
Red nucleus
- SIF:
-
Singly innervated fibers
- SO:
-
Superior olivary nucleus
- SOA:
-
Supraoculomotor area
- VI:
-
Abducens nucleus
- VIIn:
-
Facial nerve
- Vm:
-
Trigeminal motor nucleus
- WGA-HRP:
-
Wheat germ agglutinin-conjugated horseradish peroxidase
References
Adams JC (1977) Technical considerations on the use of horseradish peroxidase as a neuronal marker. Neuroscience 2(1):141–145. doi:10.1016/0306-4522(77)90074-4
Akert K, Glicksman MA, Lang W, Grob P, Huber A (1980) The Edinger–Westphal nucleus in the monkey. A retrograde tracer study. Brain Res 184(2):491–498. doi:10.1016/0006-8993(80)90816-1
Appell PP, Behan M (1990) Sources of subcortical GABAergic projections to the superior colliculus in the cat. J Comp Neurol 302(1):143–158. doi:10.1002/cne.903020111
Bachtell RK, Tsivkovskaia NO, Ryabinin AE (2002) Alcohol-induced c-Fos expression in the Edinger–Westphal nucleus: pharmacological and signal transduction mechanisms. J Pharmacol Exp Ther 302(2):516–524. doi:10.1124/jpet.102.036046
Bale TL, Vale WW (2004) CRF and CRF receptors: role in stress responsivity and other behaviors. Annu Rev Pharmacol Toxicol 44:525–557. doi:10.1146/annurev.pharmtox.44.101802.121410
Bender MB, Shanzer S (1964) Oculomotor pathways defined by electrical stimulation and lesions in the brainstem of monkey. In: Bender MB (ed) The oculomotor system. Hoeber Medical Division, Harper & Row, New York, pp 81–140
Blanks RH, Clarke RJ, Lui F, Giolli RA, Van PS, Torigoe Y (1995) Projections of the lateral terminal accessory optic nucleus of the common marmoset (Callithrix jacchus). J Comp Neurol 354(4):511–532. doi:10.1002/cne.903540404
Burde RM, Loewy AD (1980) Central origin of oculomotor parasympathetic neurons in the monkey. Brain Res 198(2):434–439. doi:10.1016/0006-8993(80)90757-X
Büttner-Ennever JA, Akert K (1981) Medial rectus subgroups of the oculomotor nucleus and their abducens internuclear input in the monkey. J Comp Neurol 197(1):17–27. doi:10.1002/cne.901970103
Büttner-Ennever JA, Horn AK, Schmidtke K (1989) Cell groups of the medial longitudinal fasciculus and paramedian tracts. Rev Neurol (Paris) 145(8–9):533–539
Büttner-Ennever JA, Cohen B, Horn AK, Reisine H (1996) Pretectal projections to the oculomotor complex of the monkey and their role in eye movements. J Comp Neurol 366(2):348–359. doi:10.1002/(SICI)1096-9861(19960304)366:2<348:AID-CNE12>3.0.CO;2-L
Büttner-Ennever JA, Horn AK, Scherberger H, D’Ascanio P (2001) Motoneurons of twitch and nontwitch extraocular muscle fibers in the abducens, trochlear, and oculomotor nuclei of monkeys. J Comp Neurol 438(3):318–335. doi:10.1002/cne.1318
Castiglioni AJ, Gallaway MC, Coulter JD (1978) Spinal projections from the midbrain in monkey. J Comp Neurol 178(2):329–346. doi:10.1002/cne.901780208
Chen B, May PJ (2000) The feedback circuit connecting the superior colliculus and central mesencephalic reticular formation: a direct morphological demonstration. Exp Brain Res 131(1):10–21. doi:10.1007/s002219900280
Cohen B, Büttner-Ennever JA (1984) Projections from the superior colliculus to a region of the central mesencephalic reticular formation (cMRF) associated with horizontal saccadic eye movements. Exp Brain Res 57(1):167–176. doi:10.1007/BF00231143
Cohen B, Matsuo V, Fradin J, Raphan T (1985) Horizontal saccades induced by stimulation of the central mesencephalic reticular formation. Exp Brain Res 57(3):605–616. doi:10.1007/BF00237847
Cohen B, Waitzman DM, Büttner-Ennever JA, Matsuo V (1986) Horizontal saccades and the central mesencephalic reticular formation. Prog Brain Res 64:243–256. doi:10.1016/S0079-6123(08)63419-6
Collewijn H, Erkelens CJ, Steinman RM (1995) Voluntary binocular gaze-shifts in the plane of regard: dynamics of version and vergence. Vision Res 35(23–24):3335–3358. doi:10.1016/0042-6989(95)00082-P
Crawford K, Terasawa E, Kaufman PL (1989) Reproducible stimulation of ciliary muscle contraction in the cynomolgus monkey via a permanent indwelling midbrain electrode. Brain Res 503(2):265–272. doi:10.1016/0006-8993(89)91673-9
Cromer JA, Waitzman DM (2006) Neurones associated with saccade metrics in the monkey central mesencephalic reticular formation. J Physiol 570(3):507–523. doi:10.1113/jphysiol.2005.096834
Cromer JA, Waitzman DM (2007) Comparison of saccade-associated neuronal activity in the primate central mesencephalic and paramedian pontine reticular formations. J Neurophysiol 98(2):835–850. doi:10.1152/jn.00308.2007
Das VE (2011) Cells in the supraoculomotor area in monkeys with strabismus show activity related to the strabismus angle. Ann N Y Acad Sci 1233:85–90. doi:10.1111/j.1749-6632.2011.06146.x
Das VE (2012) Responses of cells in the midbrain near-response area in monkeys with strabismus. Invest Ophthalmol Vis Sci 53(7):3858–3864. doi:10.1167/iovs.11-9145
Dun SL, Brailoiu GC, Mizuo K, Yang J, Chang JK, Dun NJ (2005) Neuropeptide B immunoreactivity in the central nervous system of the rat. Brain Res 1045(1–2):157–163. doi:10.1016/j.brainres.2005.03.024
Eberhorn AC, Ardeleanu P, Büttner-Ennever JA, Horn AK (2005) Histochemical differences between motoneurons supplying multiply and singly innervated extraocular muscle fibers. J Comp Neurol 491(4):352–366. doi:10.1002/cne.20715
Eberhorn AC, Büttner-Ennever JA, Horn AK (2006) Identification of motoneurons supplying multiply- or singly-innervated extraocular muscle fibers in the rat. Neuroscience 137(3):891–903. doi:10.1016/j.neuroscience.2005.10.038
Edwards SB (1975) Autoradiographic studies of the projections of the midbrain reticular formation: descending projections of nucleus cuneiformis. J Comp Neurol 161(3):341–358. doi:10.1002/cne.901610306
Edwards SB, de Olmos JS (1976) Autoradiographic studies of the projections of the midbrain reticular formation: ascending projections of nucleus cuneiformis. J Comp Neurol 165(4):417–431. doi:10.1002/cne.901650403
Edwards SB, Henkel CK (1978) Superior colliculus connections with the extraocular motor nuclei in the cat. J Comp Neurol 179(2):451–467. doi:10.1002/cne.901790212
Edwards SB, Ginsburgh CL, Henkel CK, Stein BE (1979) Sources of subcortical projections to the superior colliculus in the cat. J Comp Neurol 184(2):309–329. doi:10.1002/cne.901840207
Erichsen JT, May PJ (2002) The pupillary and ciliary components of the cat Edinger–Westphal nucleus: a transsynaptic transport investigation. Vis Neurosci 19(1):15–29. doi:10.1017/S0952523801191029
Erichsen JT, May PJ (2012) A perioculomotor nitridergic population in the macaque and cat. Invest Ophthalmol Vis Sci 53(9):5751–5761. doi:10.1167/iovs.12-10287
Erichsen JT, Wright NF, May PJ (2014) Morphology and ultrastructure of medial rectus subgroup motoneurons in the macaque monkey. J Comp Neurol 522(3):626–641. doi:10.1002/cne.23437
Erkelens CJ, Steinman RM, Collewijn H (1989) Ocular vergence under natural conditions. II. Gaze shifts between real targets differing in distance and direction. Proc R Soc Lond B Biol Sci 236(1285):441–465. doi:10.1098/rspb.1989.0030
Gamlin PD, Zhang Y, Clendaniel RA, Mays LE (1994) Behavior of identified Edinger–Westphal neurons during ocular accommodation. J Neurophysiol 72(5):2368–2382 PubMed ID: 7884465
Gaszner B, Csernus V, Kozicz T (2004) Urocortinergic neurons respond in a differentiated manner to various acute stressors in the Edinger–Westphal nucleus in the rat. J Comp Neurol 480(2):170–179. doi:10.1002/cne.20343
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 290(2):219–238. doi:10.1016/0006-8993(84)90940-5
Graf W, Gerrits N, Yatim-Dhiba N, Ugolini G (2002) Mapping the oculomotor system: the power of transneuronal labelling with rabies virus. Eur J Neurosci 15(9):1557–1562. doi:10.1046/j.1460-9568.2002.01994.x
Graham J (1977) An autoradiographic study of the efferent connections of the superior colliculus in the cat. J Comp Neurol 173(4):629–654. doi:10.1002/cne.901730403
Grantyn A, Grantyn R (1982) Axonal patterns and sites of termination of cat superior colliculus neurons projecting in the tecto-bulbo-spinal tract. Exp Brain Res 46(2):243–256. doi:10.1007/BF00237182
Gysling K, Forray MI, Haeger P, Daza C, Rojas R (2004) Corticotropin-releasing hormone and urocortin: redundant or distinctive functions? Brain Res Rev 47(1–3):116–125. doi:10.1016/j.brainresrev.2004.06.001
Handel A, Glimcher PW (1997) Response properties of saccade-related burst neurons in the central mesencephalic reticular formation. J Neurophysiol 78(4):2164–2175
Harting JK (1977) Descending pathways from the superior collicullus: an autoradiographic analysis in the rhesus monkey (Macaca mulatta). J Comp Neurol 173(3):583–612. doi:10.1002/cne.901730311
Hess A, Pilar G (1963) Slow fibers in the extraocular muscles of the cat. J Physiol 169(4):780–798. doi:10.1113/jphysiol.1963.sp007296
Hokfelt T, Blacker D, Broberger C, Herrera-Marschitz M, Snyder G, Fisone G, Cortes R, Morino P, You ZB, Ogren SO (2002) Some aspects on the anatomy and function of central cholecystokinin systems. Pharmacol Toxicol 91(6):382–386. doi:10.1034/j.1600-0773.2002.910617.x
Horn AK, Eberhorn A, Hartig W, Ardeleanu P, Messoudi A, Büttner-Ennever JA (2008) Perioculomotor cell groups in monkey and man defined by their histochemical and functional properties: reappraisal of the Edinger–Westphal nucleus. J Comp Neurol 507(3):1317–1335. doi:10.1002/cne.21598
Innis RB, Aghajanian GK (1986) Cholecystokinin-containing and nociceptive neurons in rat Edinger–Westphal nucleus. Brain Res 363(2):230–238. doi:10.1016/0006-8993(86)91008-5
Judge SJ, Cumming BG (1986) Neurons in the monkey midbrain with activity related to vergence eye movement and accommodation. J Neurophysiol 55(5):915–930
Komatsuzaki A, Alpert J, Harris HE, Cohen B (1972) Effects of mesencephalic reticular formation lesions on optokinetic nystagmus. Exp Neurol 34(3):522–534. doi:10.1016/0014-4886(72)90047-7
Kozicz T (2003) Neurons colocalizing urocortin and cocaine and amphetamine-regulated transcript immunoreactivities are induced by acute lipopolysaccharide stress in the Edinger–Westphal nucleus in the rat. Neuroscience 116(2):315–320. doi:10.1016/S0306-4522(02)00772-8
Kozicz T, Yanaihara H, Arimura A (1998) Distribution of urocortin-like immunoreactivity in the central nervous system of the rat. J Comp Neurol 391(1):1–10. doi:10.1002/(SICI)1096-9861(19980202)391:1<1:AID-CNE1>3.0.CO;2-6
Kozicz T, Li M, Arimura A (2001) The activation of urocortin immunoreactive neurons in the Einger-Westphal nucleus following stress in rats. Stress 4(2):85–90. doi:10.3109/10253890109115724
Kozicz T, Bittencourt JC, May PJ, Reiner A, Gamlin PD, Palkovits M, Horn AK, Toledo CA, Ryabinin AE (2011) The Edinger–Westphal nucleus: a historical, structural, and functional perspective on a dichotomous terminology. J Comp Neurol 519(8):1413–1434. doi:10.1002/cne.22580
Maciewicz R, Phipps BS, Foote WE, Aronin N, DiFiglia M (1983) The distribution of substance P-containing neurons in the cat Edinger–Westphal nucleus: relationship to efferent projection systems. Brain Res 270(2):217–230. doi:10.1016/0006-8993(83)90595-4
May PJ, Porter JD, Gamlin PD (1992) Interconnections between the primate cerebellum and midbrain near-response regions. J Comp Neurol 315(1):98–116. doi:10.1002/cne.903150108
May PJ, Reiner AJ, Ryabinin AE (2008a) Comparison of the distributions of urocortin containing and cholinergic neurons in the perioculomotor midbrain of the cat and macaque. J Comp Neurol 507(3):1300–1316. doi:10.1002/cne.21514
May PJ, Sun W, Erichsen JT (2008b) Defining the pupillary component of the perioculomotor preganglionic population within a unitary primate Edinger–Westphal nucleus. Prog Brain Res 171:97–106. doi:10.1016/S0079-6123(08)00613-4
May PJ, Bohlen MO, Warren S (2013) Morphology and distribution of two inputs to the oculomotor nucleus in the macaque. Soc Neurosci Abstr 39(363):03
Mays LE (1984) Neural control of vergence eye movements: convergence and divergence neurons in midbrain. J Neurophysiol 51(5):1091–1108
Mays LE, Porter JD (1984) Neural control of vergence eye movements: activity of abducens and oculomotor neurons. J Neurophysiol 52(4):743–761
Mays LE, Porter JD, Gamlin PD, Tello CA (1986) Neural control of vergence eye movements: neurons encoding vergence velocity. J Neurophysiol 56(4):1007–1021
Morley JW, Judge SJ, Lindsey JW (1992) Role of monkey midbrain near-response neurons in phoria adaptation. J Neurophysiol 67(6):1475–1492
Moschovakis AK, Karabelas AB, Highstein SM (1988a) Structure-function relationships in the primate superior colliculus. I. Morphological classification of efferent neurons. J Neurophysiol 60(1):232–262
Moschovakis AK, Karabelas AB, Highstein SM (1988b) Structure-function relationships in the primate superior colliculus. II. Morphological identity of presaccadic neurons. J Neurophysiol 60(1):263–302
Nelson JS, Goldberg SJ, McClung JR (1986) Motoneuron electrophysiological and muscle contractile properties of superior oblique motor units in cat. J Neurophysiol 55(4):715–726
Olucha F, Martinez-Garcia F, Lopez-Garcia C (1985) A new stabilizing agent for the tetramethyl benzidine (TMB) reaction product in the histochemical detection of horseradish peroxidase (HRP). J Neurosci Methods 13(2):131–138. doi:10.1016/0165-0270(85)90025-1
Pathmanathan JS, Cromer JA, Cullen KE, Waitzman DM (2006a) Temporal characteristics of neurons in the central mesencephalic reticular formation of head unrestrained monkeys. Exp Brain Res 168(4):471–492. doi:10.1007/s00221-005-0105-z
Pathmanathan JS, Presnell R, Cromer JA, Cullen KE, Waitzman DM (2006b) Spatial characteristics of neurons in the central mesencephalic reticular formation (cMRF) of head-unrestrained monkeys. Exp Brain Res 168(4):455–470. doi:10.1007/s00221-005-0104-0
Perkins E, Warren S, May PJ (2009) 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) 292(8):1162–1181. doi:10.1002/ar.20935
Perkins E, May PJ, Warren S (2014) Feed-forward and feedback projections of midbrain reticular formation neurons in the cat. Front Neuroanat 7:55. doi:10.3389/fnana.2013.00055
Phipps BS, Maciewicz R, Sandrew BB, Poletti CE, Foote WE (1983) Edinger–Westphal neurons that project to spinal cord contain substance P. Neurosci Lett 36(2):125–131. doi:10.1016/0304-3940(83)90253-7
Porter JD, Guthrie BL, Sparks DL (1983) Innervation of monkey extraocular muscles: localization of sensory and motor neurons by retrograde transport of horseradish peroxidase. J Comp Neurol 218(2):208–219. doi:10.1002/cne.902180208
Robinson FR, Phillips JO, Fuchs AF (1994) Coordination of gaze shifts in primates: brainstem inputs to neck and extraocular motoneuron pools. J Comp Neurol 346(1):43–62. doi:10.1002/cne.903460104
Ryabinin AE, Tsivkovskaia NO, Ryabinin SA (2005) Urocortin 1-containing neurons in the human Edinger–Westphal nucleus. Neuroscience 134(4):1317–1323. doi:10.1016/j.neuroscience.2005.05.042
Ryabinin AE, Tsoory MM, Kozicz T, Thiele TE, Neufeld-Cohen A, Chen A, Lowery-Gionta EG, Giardino WJ, Kaur S (2012) Urocortins: CRF’s siblings and their potential role in anxiety, depression and alcohol drinking behavior. Alcohol 46(4):349–357. doi:10.1016/j.alcohol.2011.10.007
Satoda T, Matsumoto H, Zhou L, Rose PK, Richmond FJ (2002) Mesencephalic projections to the first cervical segment in the cat. Exp Brain Res 144(3):397–413. doi:10.1007/s00221-002-1047-3
Shook BL, Schlag-Rey M, Schlag J (1990) Primate supplementary eye field: I. Comparative aspects of mesencephalic and pontine connections. J Comp Neurol 301(4):618–642. doi:10.1002/cne.903010410
Spencer RF, Porter JD (2006) Biological organization of the extraocular muscles. Prog Brain Res 151:43–80. doi:10.1016/S0079-6123(05)51002-1
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(4):493–506. doi:10.1002/cne.902710403
Sun W, May PJ (2014) Central pupillary light reflex circuits in the cat: I. The olivary pretectal nucleus. J Comp Neurol 522:3960–3977. doi:10.1002/cne.23602
Szabo J, Cowan WM (1984) A stereotaxic atlas of the brain of the cynomolgus monkey (Macaca fascicularis). J Comp Neurol 222(2):265–300. doi:10.1002/cne.902220208
Tanaka H, Yoshida T, Miyamoto N, Motoike T, Kurosu H, Shibata K, Yamanaka A, Williams SC, Richardson JA, Tsujino N, Garry MG, Lerner MR, King DS, O’Dowd BF, Sakurai T, Yanagisawa M (2003) Characterization of a family of endogenous neuropeptide ligands for the G protein-coupled receptors GPR7 and GPR8. Proc Natl Acad Sci USA 100(10):6251–6256. doi:10.1073/pnas.0837789100
Tang X, Büttner-Ennever JA, Mustari MJ, Horn AK (2015) Internal organization of medial rectus and inferior rectus muscle neurons in the C group of the oculomotor nucleus in monkey. J Comp Neurol. doi:10.1002/cne.23760
Ugolini G, Klam F, Doldan DM, Dubayle D, Brandi AM, Büttner-Ennever JA, Graf W (2006) 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 498(6):762–785. doi:10.1002/cne.21092
van Leeuwen AF, Collewijn H, Erkelens CJ (1998) Dynamics of horizontal vergence movements: interaction with horizontal and vertical saccades and relation with monocular preferences. Vision Res 38(24):3943–3954. doi:10.1016/S0042-6989(98)00092-3
Vaughan J, Donaldson C, Bittencourt J, Perrin MH, Lewis K, Sutton S, Chan R, Turnbull AV, Lovejoy D, Rivier C (1995) Urocortin, a mammalian neuropeptide related to fish urotensin I and to corticotropin-releasing factor. Nature 378(6554):287–292. doi:10.1038/378287a0
Waitzman DM, Silakov VL, Cohen B (1996) Central mesencephalic reticular formation (cMRF) neurons discharging before and during eye movements. J Neurophysiol 75(4):1546–1572
Waitzman DM, Silakov VL, DePalma-Bowles S, Ayers AS (2000a) Effects of reversible inactivation of the primate mesencephalic reticular formation. I. Hypermetric goal-directed saccades. J Neurophysiol 83(4):2260–2284
Waitzman DM, Silakov VL, DePalma-Bowles S, Ayers AS (2000b) Effects of reversible inactivation of the primate mesencephalic reticular formation. II. Hypometric vertical saccades. J Neurophysiol 83(4):2285–2299
Waitzman DM, Van Horn MR, Cullen KE (2008) Neuronal evidence for individual eye control in the primate cMRF. Prog Brain Res 171:143–150. doi:10.1016/S0079-6123(08)00619-5
Wang N, Warren S, May PJ (2010) The macaque midbrain reticular formation sends side-specific feedback to the superior colliculus. Exp Brain Res 201(4):701–717. doi:10.1007/s00221-009-2090-0
Wang N, Perkins E, Zhou L, Warren S, May PJ (2013) Anatomical evidence that the superior colliculus controls saccades through central mesencephalic reticular formation gating of omnipause neuron activity. J Neurosci 33(41):16285–16296. doi:10.1523/JNEUROSCI.2726-11.2013
Warren S, Waitzman DM, May PJ (2008) Anatomical evidence for interconnections between the central mesencephalic reticular formation and cervical spinal cord in the cat and macaque. Anat Rec (Hoboken) 291(2):141–160. doi:10.1002/ar.20644
Warwick R (1954) The ocular parasympathetic nerve supply and its mesencephalic sources. J Anat 88(1):71–93
Wasicky R, Horn AK, Büttner-Ennever JA (2004) Twitch and nontwitch motoneuron subgroups in the oculomotor nucleus of monkeys receive different afferent projections. J Comp Neurol 479(2):117–129. doi:10.1002/cne.20296
Weitemier AZ, Ryabinin AE (2006) Urocortin 1 in the dorsal raphe regulates food and fluid consumption, but not ethanol preference in C57BL/6 J mice. Neuroscience 137(4):1439–1445. doi:10.1016/j.neuroscience.2005.10.021
Yamamoto H, Maeda T, Fujimura M, Fujimiya M (1998) Urocortin-like immunoreactivity in the substantia nigra, ventral tegmental area and Edinger–Westphal nucleus of rat. Neurosci Lett 243(1–3):21–24. doi:10.1016/S0304-3940(98)00071-8
Zhang Y, Mays LE, Gamlin PD (1992) Characteristics of near response cells projecting to the oculomotor nucleus. J Neurophysiol 67(4):944–960
Zhou L, Warren S, May PJ (2008) The feedback circuit connecting the central mesencephalic reticular formation and the superior colliculus in the macaque monkey: tectal connections. Exp Brain Res 189(4):485–496. doi:10.1007/s00221-008-1444-3
Acknowledgments
This work was supported by the National Institutes of Health, National Eye Institute grant EY014263 to Paul J. May, PhD and Susan Warren, PhD. We are grateful to Jinrong Wei for her technical support in the histological processing of the tissue.
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The authors declare that they have no conflicts of interest pursuant to the publication of this research.
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Bohlen, M.O., Warren, S. & May, P.J. A central mesencephalic reticular formation projection to the supraoculomotor area in macaque monkeys. Brain Struct Funct 221, 2209–2229 (2016). https://doi.org/10.1007/s00429-015-1039-2
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DOI: https://doi.org/10.1007/s00429-015-1039-2