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The feedback circuit connecting the central mesencephalic reticular formation and the superior colliculus in the macaque monkey: tectal connections

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Abstract

The connectional and physiological characteristics of the central mesencephalic reticular formation (cMRF) indicate that it participates in gaze control. The cMRF receives projections from the ipsilateral superior colliculus (SC) via collaterals of predorsal bundle axons. These collaterals target cMRF neurons, which in turn project back upon the SC. In the present study, we examined the pattern of connections made by the cMRF reticulotectal projection by injecting the bidirectional neuroanatomical tracer, biotinylated dextran amine (BDA), into the cMRF of macaque monkeys. Anterogradely labeled reticulotectal terminals were found bilaterally in the SC, with an ipsilateral predominance, and were concentrated in the intermediate gray layer (SGI). BDA also retrogradely labeled SC neurons projecting to the cMRF. These labeled tectoreticular cells were located mainly in SGI. Injection site specific differences in the SC labeling pattern were evident, suggesting the lateral cMRF is more heavily connected to the upper sublamina of SGI, whereas the medial cMRF is more heavily connected with the lower sublamina. In view of the known downstream connections of the cMRF and these SC sublaminae, this organization intimates that the cMRF may contain subdivisions specialized to modulate the eye and the head components of gaze changes. In addition, reticulotectal terminals were observed to have close associations with retrogradely labeled tectoreticular cells in the ipsilateral SC, indicating possible synaptic contacts. Thus, the cMRF’s reciprocal connections with the SC suggest this structure plays a role in defining the gaze-related bursting behavior of collicular output neurons.

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References

  • Appell PP, Behan M (1990) Sources of subcortical GABAergic projections to the superior colliculus in the cat. J Comp Neurol 302:143–158

    Article  PubMed  CAS  Google Scholar 

  • Behan M (1985) An EM-autoradiographic and EM-HRP study of the commissural projection of the superior colliculus in the cat. J Comp Neurol 234:105–116

    Article  PubMed  CAS  Google Scholar 

  • Castiglioni AJ, Gallaway MC, Coulter JD (1978) Spinal projections from the midbrain in monkey. J Comp Neurol 178:329–346

    Article  PubMed  CAS  Google Scholar 

  • Chen B, May PJ (2000) The feedback circuit connecting the superior colliculus and central mesencephalic reticular formation: a direct morphological demonstration. Exp Brain Res 131:10–21

    Article  PubMed  CAS  Google Scholar 

  • 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 57:167–176

    Article  PubMed  CAS  Google Scholar 

  • Cohen B, Matsuo V, Fradin J, Raphan T (1985) Horizontal saccades induced by stimulation of the central mesencephalic reticular formation. Exp Brain Res 57:605–616

    Article  PubMed  CAS  Google Scholar 

  • Corneil BD, Olivier E, Richmond FJ, Loeb GE, Munoz DP (2001) Neck muscles in the rhesus monkey. II. Electromyographic patterns of activation underlying postures and movements. J Neurophysiol 86:1729–1749

    PubMed  CAS  Google Scholar 

  • Cowie RJ, Robinson D (1994) Subcortical contributions to head movements in macaques. 1. Contrasting effects of electrical stimulation of a medial pontomedullary region and the superior colliculus. J Neurophysiol 72:2648–2664

    PubMed  CAS  Google Scholar 

  • Cromer JA, Waitzman DM (2006) Neurones associated with saccade metrics in the monkey central mesencephalic reticular formation. J Physiol 570:507–523

    Article  PubMed  CAS  Google Scholar 

  • Cromer JA, Waitzman DM (2007) Comparison of saccade-associated neuronal activity in the primate central mesencephalic and paramedian pontine reticular formations. J Neurophysiol 98:835–850

    Article  PubMed  Google Scholar 

  • Edwards SB, de Olmos JS (1976) Autoradiographic studies of the projections of the midbrain reticular formation: ascending projection of nucleus cuneiformis. J Comp Neurol 165:417–432

    Article  PubMed  CAS  Google Scholar 

  • Edwards SB, Ginsburgh CL, Henkel CK, Stein BE (1979) Sources of subcortical projections to the superior colliculus in the cat. J Comp Neurol 184:309–329

    Article  PubMed  CAS  Google Scholar 

  • Freedman EG, Sparks DL (1997) Activity of cells in the deeper layers of the superior colliculus of the rhesus monkey: evidence for a gaze displacement command. J Neurophysiol 78:1669–1690

    PubMed  CAS  Google Scholar 

  • Fuentes-Santamaria V, Alvarado JC, Stein BE, McHaffie JG (2007) Cortex contacts both output neurons and nitrergic interneurons in the superior colliculus: Direct and indirect routes for multisensory integration. Cereb Cortex (in press)

  • Fuller JH (1992) Head movement propensity. Exp Brain Res 92:152–164

    Article  PubMed  CAS  Google Scholar 

  • Goosens HH, Van Opstal AJ (1997) Human eye-head coordination in two dimensions under different sensorimotor conditions. Exp Brain Res 114:542–560

    Article  Google Scholar 

  • 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 46:243–256

    Article  PubMed  CAS  Google Scholar 

  • Handel A, Glimcher PW (1997) Response properties of saccade-related burst neurons in the central mesencephalic reticular formation. J Neurophysiol 78:2164–2175

    PubMed  CAS  Google Scholar 

  • Harting JK (1977) Descending pathways from the superior colliculus: an autoradiographic analysis in the rhesus monkey (Macaca mulatta). J Comp Neurol 173:583–612

    Article  PubMed  CAS  Google Scholar 

  • Luque MA, Pérez- Pérez MP, Herrero L, Torres B (2005) Involvement of the optic tectum and mesencephalic reticular formation in the generation of saccadic eye movements in goldfish. Brain Res Rev 49:388–397

    Article  Google Scholar 

  • May PJ (2006) The mammalian superior colliculus: laminar structure and connections. Prog Brain Res 151:321–378

    Article  PubMed  Google Scholar 

  • May PJ, Porter JD (1992) The laminar distribution of macaque tectobulbar and tectospinal neurons. Vis Neurosci 8:257–276

    Article  PubMed  CAS  Google Scholar 

  • May PJ, Warren S, Chen B, Richmond FJR, Olivier E (2002) Midbrain reticular formation circuitry subserving gaze in the cat. Ann N Y Acad Sci 956:405–408

    PubMed  Google Scholar 

  • Mize RR (1996) Neurochemical microcircuitry underlying visual and oculomotor function in the cat superior colliculus. Prog Brain Res 112:35–55

    Article  PubMed  CAS  Google Scholar 

  • Moschovakis AK, Karabelas AB, Highstein SM (1988a) Structure-function relationships on the primate superior colliculus. I. Morphological classification of efferent neurons. J Neurophysiol 60:232–262

    PubMed  CAS  Google Scholar 

  • Moschovakis AK, Karabelas AB, Highstein SM (1988b) Structure-function relationships in the primate superior colliculus. II. Morphological identity of presaccadic neurons. J Neurophysiol 60:263–298

    PubMed  CAS  Google Scholar 

  • Moschovakis AK, Kitama T, Dalzios Y, Petit J, Brandi AM, Grantyn AA (1998) An anatomical substrate for the spatiotemporal transformation. J Neurosci 18:10219–10229

    PubMed  CAS  Google Scholar 

  • Munoz DP, Istevan PJ (1998) Lateral inhibitory interactions in the intermediate layers of the monkey superior colliculus. J Neurophysiol 79:1193–1209

    PubMed  CAS  Google Scholar 

  • Munoz DP, Guitton D, Pelisson D (1991) Control of orienting gaze shifts by the tectoreticulospinal system in the head-free cat. III. Spatiotemporal characteristics of phasic motor discharges. J Neurophysiol 66:1642–1666

    PubMed  CAS  Google Scholar 

  • Olivier E, Porter JD, May PJ (1998) Comparison of the distribution and somatodendritic morphology of tectotectal neurons in the cat and monkey. Vis Neurosci 15:903–922

    Article  PubMed  CAS  Google Scholar 

  • Pathmanathan JS, Presnell R, Cromer JA, Cullen KE, Waitzman DM (2006a) Spatial characteristics of neurons in the central mesencephalic reticular formation (cMRF) of head-unrestrained monkeys. Exp Brain Res 168:455–470

    Article  PubMed  Google Scholar 

  • Pathmanathan JS, Cromer JA, Cullen KE, Waitzman DM (2006b) Temporal characteristics of neurons in the central mesencephalic reticular formation of head unrestrained monkeys. Exp Brain Res 168:471–492

    Article  PubMed  Google Scholar 

  • Paxinos G, Huang X-F, Toga AW (2000) The Rhesus Monkey Brain in Stereotaxic Coordinates. Academic Press, San Diego

    Google Scholar 

  • Pérez- Pérez MP, Luque MA, Herrero L, Nunez-Abades PA, Torres B (2003) Connectivity of the goldfish optic tectum with the mesencephalic and rhomencephalic reticular formation. Exp Brain Res 151:123–135

    Article  PubMed  Google Scholar 

  • Robinson FR, Phillips JO, Fuchs AF (1994) Coordination of gaze shifts in primates: brainstem inputs to neck and extraocular motoneuron pools. J Comp Neurol 346:43–62

    Article  PubMed  CAS  Google Scholar 

  • Roucoux A, Crommelinck M, Decostre MF (1989) Neck muscle activity in eye-head coordinated movements. Prog Brain Res 80:351–62

    Article  PubMed  CAS  Google Scholar 

  • Stahl JS (2001) Eye-head coordination and the variation of eye-movement accuracy with orbital eccentricity. Exp Brain Res 36:200–210

    Article  Google Scholar 

  • Stryker MP, Schiller PH (1975) Eye and head movements evoked by electrical stimulation of monkey superior colliculus. Exp Brain Res 23:103–112

    Article  PubMed  CAS  Google Scholar 

  • Takahashi M, Sugiuchi Y, Izawa Y, Shinoda Y (2005) Commissural excitation and inhibition by the superior colliculus in tectoreticular neurons projecting to omnipause neuron and inhibitory burst neuron regions. J Neurophysiol 94:1707–1726

    Article  PubMed  CAS  Google Scholar 

  • Ugolini G, Klam F, Dans MD, Dubayle D, Brandi AM, Büttner-Ennever J, 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 498:762–785

    Article  PubMed  Google Scholar 

  • Waitzman DM, Silakov VL, Cohen B (1996) Central mesencephalic reticular formation (cMRF) neurons discharging before and during eye movements. J Neurophysiol 75:1546–1572

    PubMed  CAS  Google Scholar 

  • Waitzman DM, Silakov VL, DePalma-Bowles S, Ayers AS (2000) Effects of reversible inactivation of the primate mesencephalic reticular formation. I. Hypermetric goal-directed saccades. J Neurophysiol 83:2260–2284

    PubMed  CAS  Google Scholar 

  • Walton MMG, Bechara B, Gandhi NJ (2007) Role of primate superior colliculus in the control of head movements. J Neurophys 98:2022–2037

    Article  Google Scholar 

  • 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 291:141–160

    Article  Google Scholar 

  • Wurtz RH, Goldberg ME (1972) Activity of superior colliculus in behaving monkey. 3. Cells discharging before eye movements. J Neurophysiol 35:575–586

    PubMed  CAS  Google Scholar 

  • Zhou L, Warren S, May PJ (2006) Projection of the central mesencephalic reticular formation in the macaque. Soc Neurosci Abst 32:139.1

    Google Scholar 

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Acknowledgments

The authors are grateful to Dr. Olga Golanov for her excellent histological work and help in the production of the figures. We are indebted to Dr. John McHaffie for his thoughtful comments on an earlier draft of this work.

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Correspondence to Paul J. May.

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Zhou, L., Warren, S. & May, P.J. The feedback circuit connecting the central mesencephalic reticular formation and the superior colliculus in the macaque monkey: tectal connections. Exp Brain Res 189, 485–496 (2008). https://doi.org/10.1007/s00221-008-1444-3

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  • DOI: https://doi.org/10.1007/s00221-008-1444-3

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