Oculomotor areas of the primate frontal lobes: A transneuronal transfer of rabies virus and [14C]-2-deoxyglucose functional imaging study

Journal of Neuroscience

Volumn 24, Issue 25, 2004, Pages 5726-5740

  Moschovakis, A K ^a   Gregoriou, G G ^a   Ugolini, G ^b   Doldan, M ^b   Graf, W ^c   Guldin, W ^d   Hadjidimitrakis, K ^a   Savaki, H E ^a  

^a UNIVERSITY OF CRETE   (Greece)

^b LABORATOIRE DE NEUROBIOLOGIE CELLULAIRE ET MOLÉCULAIRE   (France)

^c CNRS   (France)

^d University of Landau   (Germany)

Author keywords

Cingulate eye fields; Frontal eye field; Oculomotor; Principal sulcus; Saccades; Supplementary eye field

Indexed keywords

DEOXYGLUCOSE; DEOXYGLUCOSE C 14; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARCUATE NUCLEUS; ARTICLE; BRAIN METABOLISM; CINGULATE GYRUS; DORSOMEDIAL FRONTAL CORTEX; EYE FIXATION; EYE MOVEMENT; FEMALE; FRONTAL CORTEX; FRONTAL LOBE; FUNCTIONAL NEUROIMAGING; GLUCOSE UTILIZATION; ISOTOPE LABELING; LIMBIC CORTEX; MACACA; MOTONEURON; NERVE PROJECTION; NEUROIMAGING; NONHUMAN; OCULOMOTOR SYSTEM; ORBITAL CORTEX; PREMOTOR CORTEX; PRIORITY JOURNAL; RABIES VIRUS; RETROGRADE NERVE FIBER TRANSPORT; SACCADIC EYE MOVEMENT; VIRUS TRANSNEURONAL TRANSFER; VISUAL FIELD;

ANIMALS; DEOXYGLUCOSE; FEMALE; FIXATION, OCULAR; FRONTAL LOBE; MACACA FASCICULARIS; MACACA MULATTA; MOTOR NEURONS; NEURAL PATHWAYS; OCULOMOTOR MUSCLES; RABIES VIRUS; SACCADES;

EID: 3042773255     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1223-04.2004     Document Type: Article

References (80)

1. Anderson TJ, Jenkins IH, Brooks DJ, Hawken MB, Frackowiak RSJ, Kennard C (1994) Cortical control of saccades and fixation in man. A PET study. Brain 117:1073-1084.
2. Azuma M, Nakayama H, Sasaki Y, Suzuki H (1988) Relation between visual input and motor outflow for eye movements in monkey visual field. Behav Brain Res 27:93-98.
3. Barbas H, Pandya DN (1987) Architecture and frontal cortical connections of the premotor cortex (area 6) in the rhesus monkey. J Comp Neurol 256:211-228.
4. Barbas H, Ghashghaei H, Dombrowski SM, Rempel-Clower NL (1999) Medial prefrontal cortices are unified by common connections with superior temporal cortices and distinguished by input from memory-related areas in the rhesus monkey. J Comp Neurol 410:343-367.
5. Bates JF, Goldman-Rakic PS (1993) Prefrontal connections of medial motor areas in the rhesus monkey. J Comp Neurol 311:211-228.
6. Bizzi E (1968) Discharge of frontal eye field neurons during saccadic and following eye movements in unanesthetized monkeys. Exp Brain Res 6:69-80.
7. Boch R, Goldberg ME (1989) Participation of prefrontal neurons in the preparation of visually guided eye movements in the rhesus monkey. J Neurophysiol 61:1064-1084.
8. Bon L, Lucchetti C (1992) The dorsomedial frontal cortex of the macaca monkey: fixation and saccade related activity. Exp Brain Res 89:571-580.
9. Bon L, Lucchetti C (1994) Ear and eye representation in the frontal cortex, area 8b, of the macaque monkey: an electrophysiological study. Exp Brain Res 102:259-271.
10. Bruce CJ, Goldberg ME (1985) Primate frontal eye fields. I. Single neurons discharging before saccades. J Neurophysiol 53:603-635.
11. Bruce CJ, Goldberg ME, Stanton GB, Bushnell MC (1985) Primate frontal eye fields. II. Physiological and anatomical correlates of electrically evoked eye movements. J Neurophysiol 54:714-734.
12. Dalezios Y, Raos VC, Savaki HE (1996) Metabolic activity pattern in the motor and somatosensory cortex of monkeys performing a visually guided reaching task with one forelimb. Neuroscience 72:325-333.
13. Dias EC, Kiesau M, Segraves MA (1995) Acute activation and inactivation of macaque frontal eye field with GABA-related drugs. J Neurophysiol 74:2744-2748.
14. Doricchi F, Perani D, Incoccia C, Grassi F, Cappa SF, Bettinardi V, Galati G, Pizzamiglio L, Fazio F (1997) Neural control of fast-regular saccades and antisaccades: an investigation using positron emission tomography. Exp Brain Res 116:50-62.
15. Fox PT, Fox JM, Raichle ME, Burde RM (1985) The role of cerebral cortex in the generation of voluntary saccades: a positron emission tomographic study. J Neurophysiol 54:348-369.
16. Fries W (1984) Cortical projections to the superior colliculus in the macaque monkey: a retrograde study using horseradish peroxidase. J Comp Neurol 230:55-76.
17. Fujii N, Mushiake H, Tamai M, Tanji J (1995) Microstimulation of the supplementary eye field during saccade preparation. NeuroReport 18:2565-2568.
18. Fujii N, Mushiake H, Tanji J (1998) An oculomotor representation area within the ventral premotor cortex. Proc Natl Acad Sci USA 95:12034-12037.
19. Fukushima K, Yamanobe T, Shinmei Y, Fukushima J, Kurkin S, Peterson BW (2002) Coding of smooth eye movements in three-dimensional space by frontal cortex. Nature 419:157-162.
20. Funahashi S, Bruce CJ, Goldman-Rakic PS (1991) Neuronal activity related to saccadic eye movements in the monkey's dorsolateral prefrontal cortex. J Neurophysiol 65:1464-1483.
21. Funahashi S, Bruce CJ, Goldman-Rakic PS (1993) Dorsolateral prefrontal lesions and oculomotor delayed-response performance: evidence for mnemonic "scotomas." J Neurosci 13:1479-1497.
22. Gamlin PD, Yoon K (2000) An area for vergence eye movement in primate frontal cortex. Nature 407:1003-1007.
23. Gaymard B, Rivaud S, Cassarini JF, Dubard T, Rancurel G, Agid Y, Pierrot-Deseilligny C (1998) Effects of anterior cingulate cortex lesions on ocular saccades in humans. Exp Brain Res 120:173-183.
24. Ghosh S, Gattera R (1995) A comparison of the ipsilateral cortical projections to the dorsal and ventral subdivisions of the macaque premotor cortex. Somatosens Mot Res 12:359-378.
25. Graf W, Klam F, Ugolini G (1999) Retrograde transneuronal labeling with rabies virus of horizontal eye movement circuits in primates. Soc Neurosci Abstr 25:1651.
26. Graf W, Dubayle D, Klam F, Biarnais T, Büttner-Ennever J, Ugolini G (2000) Horizontal eye movement network in primates. I. Monosynaptic input. Soc Neurosci Abstr 26:969.
27. 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 15:1557-1562.
28. Grantyn A, Brandi A-M, Dubayle D, Graf W, Ugolini G, Hadjidimitrakis K, Moschovakis A (2002) Density gradients of trans-synaptically labeled collicular neurons after injections of rabies virus in the lateral rectus muscle of the rhesus monkey. J Comp Neurol 451:346-361.
29. Gregoriou GG, Savaki HE (2001) The intraparietal cortex: subregions involved in fixation, saccades and in the visual and somatosensory guidance of reaching. J Cereb Blood Flow Metab 21:671-682.
30. Gregoriou GG, Savaki HE (2003) When vision guides movement: a functional imaging study of the monkey brain. NeuroImage 19:959-967.
31. Guldin W, Dahrmann G, Doldan M, Graf W, Bäurle J, Moschovakis A, Ugolini G (2000) Horizontal eye movement network in primates. III. Cortical relays. Soc Neurosci Abstr 26:969.
32. Hubel DH, Wiesel TN (1972) Laminar and columnar distribution of geniculo-cortical fibers in the macaque monkey. J Comp Neurol 146:421-450.
33. Huerta MF, Kaas JH (1990) Supplementary eye field as defined by intracortical microstimulation: connections in macaques. J Comp Neurol 293:299-330.
34. Huerta MF, Krubitzer LA, Kaas JH (1986) Frontal eye field as defined by intracortical microstimulation in squirrel monkeys, owl monkeys, and macaque monkey. I. Subcortical connections. J Comp Neurol 253:415-439.
35. Joseph JP, Barone P (1987) Prefrontal unit activity during a delayed oculomotor task in the monkey. Exp Brain Res 67:460-468.
36. Kennedy C, Sakurada O, Shinohara M, Jehle J, Sokoloff L (1978) Local cerebral glucose utilization in the normal conscious macaque monkey. Ann Neurol 4:293-301.
37. Langer T, Kaneko CRS, Scudder CA, Fuchs AF (1986) Afferents to the abducens nucleus in the monkey and cat. J Comp Neurol 245:379-400.
38. Leichnetz GR, Spencer RF, Hardy SGP, Astruc J (1981) The prefrontal corticotectal projection in the monkey: an anterograde and retrograde horseradish peroxidase study. Neuroscience 6:1023-1041.
39. Luppino G, Matelli M, Camarda RM, Gallese V, Rizzolatti G (1991) Multiple representations of body movements in mesial area 6 and the adjacent cingulate cortex: an intracortical microstimulation study in the macaque monkey. J Comp Neurol 311:463-482.
40. MacAvoy MG, Gottleib JP, Bruce CJ (1991) Smooth-pursuit eye movement representation in the primate frontal eye field. Cereb Cortex 1:95-102.
41. Matelli M, Luppino G, Rizzolatti G (1985) Patterns of cytochrome oxidase activity in the frontal agranular cortex of the macaque monkey. Behav Brain Res 18:125-136.
42. Matelli M, Luppino G, Rizzolatti G (1991) Architecture of superior and mesial area 6 and the adjacent cingulate cortex in the macaque monkey. J Comp Neurol 311:445-462.
43. Morcuende S, Delgado-García JM, Ugolini G (2002) Neuronal premotor networks involved in eyelid responses: retrograde transneuronal tracing with rabies virus from the orbicularis oculi muscle in the rat. J Neurosci 22:8808-8818.
44. Moschovakis AK, Scudder CA, Highstein SM (1996) The microscopic anatomy and physiology of the mammalian saccadic system. Progr Neurobiol 50:133-254.
45. Moschovakis AK, Gregoriou GG, Savaki HE (2001) Functional imaging of the primate superior colliculus during saccades to visual targets. Nat Neurosci 4:1026-1031.
46. Nguyen LT, Spencer RF (1999) Abducens internuclear and ascending tract of Deiters inputs to medial rectus motoneurons in the cat oculomotor nucleus: neurotransmitters. J Comp Neurol 411:73-86.
47. O'Driscoll GA, Alpert NM, Matthysse SW, Levy DL, Rauch SL, Holzman PS (1995) Functional neuroanatomy of antisaccade eye movements investigated with positron emission tomography. Proc Natl Acad Sci USA 92:925-929.
48. Paus T (1991) Medial versus lateral frontal lobe lesions and differential impairment of central gaze fixation maintenance in man. Brain 114:2051-2067.
49. Paus T, Marrett S, Worsley KJ, Evans AC (1995) Extraretinal modulation of cerebral blood flow in the human visual cortex: implications for saccadic suppression. J Neurophysiol 74:2179-2183.
50. Petit L, Orssaud C, Tzourio N, Salamon G, Mazoyer B, Berthoz A (1993) PET study of voluntary saccadic eye movements in humans: basal ganglia- thalamocortical system and cingulate cortex involvement. J Neurophysiol 69:1009-1017.
51. Petit L, Tzourio N, Orssaud C, Pietrzyk U, Berthoz A, Mazoyer B (1995) Functional neuroanatomy of the human visual fixation system. Eur J Neurosci 7:169-174.
52. Petit L, Orssaud C, Tzourio N, Crivello F, Berthoz A, Mazoyer B (1996) Functional anatomy of a prelearned sequence of horizontal saccades in humans. J Neurosci 16:3714-3726.
53. Raos V, Franchi G, Galesse V, Fagassi L (2003) Somatotopic organization of the lateral part of area F2 (dorsal premotor cortex) of the macaque monkey. J Neurophysiol 89:1503-1518.
54. Remmel RS (1984) An inexpensive eye movement monitor using the sclera coil technique. IEEE Trans Biomed Engin 4:388-390.
55. Rizzolatti G, Camadra R, Fogassi L, Gentilucci M, Luppino G, Matelli M (1988) Functional organization of inferior area 6 in the macaque monkey. II. Area F5 and the control of distal movements. Exp Brain Res 71:491-507.
56. Robinson DA, Fuchs AF (1969) Eye movements evoked by stimulation of frontal eye fields. J Neurophysiol 32:637-648.
57. Romanski LM, Giguere M, Bates JF, Goldman-Rakic PS (1997) Topographic organization of medial pulvinar connections with the prefrontal cortex in the rhesus monkey. J Comp Neurol 379:313-332.
58. Russo GS, Bruce CJ (1993) Effect of eye position within the orbit on electrically elicited saccadic eye movements: a comparison of the macaque monkey's frontal and supplementary eye fields. J Neurophysiol 69:800-818.
59. Russo GS, Bruce CJ (2000) Supplementary eye field: representation of saccades and relationship between neural response fields and elicited eye movements. J Neurophysiol 84:2605-2621.
60. Savaki HE, Kennedy C, Sokoloff L, Mishkin M (1993) Visually guided reaching with the forelimb contralateral to a "blind" hemisphere: a metabolic mapping study in monkeys. J Neurosci 13:2772-2789.
61. Savaki HE, Raos VC, Dalezios Y (1997) Spatial cortical patterns of metabolic activity in monkeys performing a visually guided reaching task with one forelimb. Neuroscience 76:1007-1034.
62. Schall JD (1991) Neuronal activity related to visually guided saccadic eye movements in the supplementary motor area of rhesus monkeys. J Neurophysiol 66:530-558.
63. Schall JD, Morel A, Kaas JH (1993) Topography of supplementary eye field afferents to frontal eye field in macaque: implications for mapping between saccade coordinate systems. Vis Neurosci 10:385-393.
64. Schlag J, Schlag-Rey M (1987) Evidence for a supplementary eye field. J Neurophysiol 57:179-200.
65. Schnyder H, Reisine H, Hepp K, Henn V (1985) Frontal eye field projection to the paramedian pontine reticular formation traced with wheat germ aggluttinin in the monkey. Brain Res 329:151-160.
66. Shook BL, Schlag-Rey M, Schlag J (1988) Direct projections from the supplementary eye field to the nucleus raphe interpositus. Exp Brain Res 73:215-218.
67. Shook BL, Schlag-Rey M, Schlag J (1990) Primate supplementary eye field. I. Comparative aspects of mesencephalic and pontine connections. J Comp Neurol 301:618-642.
68. Sokoloff L (1977) Relation between physiological function and energy metabolism in the central nervous system. J Neurochem 29:13-26.
69. 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 271:493-506.
70. Suzuki H, Azuma M (1977) Prefrontal neuronal activity during gazing at a light spot in the monkey. Brain Res 126:497-508.
71. Sweeney JA, Mintun MA, Kwee S, Wiseman MB, Brown DL, Rosenberg DR, Carl JR (1996) Positron emission tomography study of voluntary saccadic eye movements and spatial working memory. J Neurophysiol 75:454-468.
72. Talairach J, Bancaud J, Geier S, Bordas-Ferrer M, Bonis A, Szikla G, Rusu M (1973) The cingulate cortex and human behavior. Electroencephalogr Clin Neurophysiol 34:45-52.
73. Tanaka M, Lisberger SG (2002) Role of arcuate frontal cortex of monkeys in smooth pursuit eye movements. I. Basic response properties to retinal image motion and position. J Neurophysiol 87:2684-2699.
74. Tang Y, Rampin O, Giuliano F, Ugolini G (1999) Spinal and brain circuits to motoneurons of the bulbospongiosus muscle: retrograde transneuronal tracing with rabies virus. J Comp Neurol 414:167-192.
75. Tehovnik EJ, Lee K (1993) The dorsomedial frontal cortex of the rhesus monkey: topographic representation of saccades evoked by electrical stimulation. Exp Brain Res 96:430-442.
76. Ugolini G (1995) Specificity of rabies virus as a transneuronal tracer of motor networks: transfer from hypoglossal motoneurons to connected second-order and higher order central nervous system cell groups. J Comp Neurol 356:457-480.
77. Ugolini G, Dubayle D, Grantyn A, Brandi A, Berthoz A, Büttner-Ennever J, Moschovakis A, Graf W (2000) Horizontal eye movement network in primates. II. Polysynaptic input. Soc Neurosci Abstr 26:969.
78. Ugolini G, Büttner-Ennever J, Doldan M, Dubayle D, Klam F, Graf W (2001) Horizontal eye movement networks in primates: differences in monosynaptic input to slow and fast abducens motoneurons. Soc Neurosci Abstr 27:403-13.
79. Walker AE (1940) A cytoarchitectonic study of the prefrontal area of the macaque monkey. J Comp Neurol 73:59-86.
80. Yeterian EH, Pandya DN (1988) Corticothalamic connections of paralimbic regions in the rhesus monkey. J Comp Neurol 269:130-146.