Topography of visual cortex connections with frontal eye field in macaque: Convergence and segregation of processing streams

Journal of Neuroscience

Volumn 15, Issue 6, 1995, Pages 4464-4487

  Schall, Jeffrey D ^a   Morel, Anne ^b   King, Dana J ^a   Bullier, Jean ^c  

^a VANDERBILT UNIVERSITY   (United States)

^b UNIVERSITY HOSPITAL ZURICH   (Switzerland)

^c INSERM   (France)

Author keywords

extrastriate cortex; eye movement; frontal cortex; frontal eye field; oculomotor system; parallel pathways; saccade; visual cortex; visual system

Indexed keywords

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; MONKEY; NONHUMAN; OCULOMOTOR SYSTEM; PARIETAL LOBE; PERCEPTION; PRIORITY JOURNAL; SACCADIC EYE MOVEMENT; SPATIAL DISCRIMINATION; VISUAL CORTEX;

EID: 0029003587     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.15-06-04464.1995     Document Type: Article

References (108)

1. Andersen RA, Asanuma C, Cowan WM (1985) Callosal and prefrontal associational projecting cell populations in area 7A of the macaque monkey: a study using retrogradely transported fluorescent dyes. J Comp Neurol 232:443-455.
2. Andersen RA, Asanuma C, Essick G, Siegel RM (1990a) Corticocortical connections of anatomically and physiologically defined subdivisions within the inferior parietal lobule. J Comp Neurol 296:65-113.
3. Andersen RA, Bracewell M, Barash S, Gnadt J, Fogassi L (1990b) Eye position effects on visual, memory and saccade-related activity in areas LIP and 7a of macaque. J Neurosci 10:1176-1196.
4. Arikuni T, Watanabe K, Kubota K (1988) Connections of area 8 with area 6 in the brain of the macaque monkey. J Comp Neurol 277:21-40.
5. Azuma M, Suzuki H (1984) Properties and distribution of auditory neurons in the dorsolateral prefrontal cortex of the alert monkey. Brain Res 298:343-346.
6. Bahill AT, Adler D, Stark L (1975) Most naturally occurring human saccades have magnitudes of 15 deg or less. Invest Ophthalmol 14: 468-469.
7. Baizer JS, Ungerleider LG, Desimone R (1991) Organization of visual inputs to the inferior temporal and posterior parietal cortex in macaques. J Neurosci 11:168-190.
8. Barbas H (1988) Anatomic organization of basoventral and mediodorsal visual recipient prefrontal regions in the rhesus monkey. J Comp Neurol 276:313-342.
9. Barbas H, Mesulam M-M (1981) Organization of afferent input to subdivisions of area 8 in the rhesus monkey. J Comp Neurol 200: 407-431.
10. Baylis GC, Rolls ET, Leonard CM (1987) Functional subdivisions of the temporal lobe neocortex. J Neurosci 7:330-342.
11. Blatt GJ, Andersen RA, Stoner GR (1990) Visual receptive field organization and cortico-cortical connections of the lateral intraparietal area (area LIP) in the macaque. J Comp Neurol 299:421-445.
12. Boussaoud D, Ungerleider LG, Desimone R (1990) Pathways for motion analysis: cortical connections of the medial superior temporal and fundus of the superior temporal visual areas in the macaque. J Comp Neurol 296:462-495.
13. Boussaoud D, Desimone R, Ungerleider LG (1991) Visual topography of area TEO in the macaque. J Comp Neurol 306:554-575.
14. Bruce CJ, Goldberg ME (1985) Primate frontal eye fields. I. Single neurons discharging before saccades. J Neurophysiol 53:603-635.
15. Bruce CJ, Russo GS (1987) Effects of ketamine on oculomotor function in the monkey. Soc Neurosci Abstr 13:171.
16. Bruce CJ, Desimone R, Gross CG (1981) Visual properties of neurons in a polysensory area in superior temporal sulcus of the macaque. J Neurophysiol 46:369-384.
17. 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 54:714-734.
18. Burkhalter A, Felleman DJ, Newsome WT, Van Essen DC (1986) Anatomical and physiological asymmetries related to visual areas V3 and VP in macaque extrastriate cortex. Vision Res 26:63-80.
19. Cavada C, Goldman-Rakic PS (1989) Posterior parietal cortex in rhesus monkey: II. Evidence for segregated corticocortical networks linking sensory and limbic areas with the frontal lobe. J Comp Neurol 287:422-445.
20. Cave KR, Wolfe JM (1990) Modeling the role of parallel processing in visual search. Cognit Psychol 22:225-271.
21. Chelazzi L, Miller EK, Duncan J, Desimone, R (1993) A neural basis for visual search in inferior temporal cortex. Nature 363:345-347.
22. Colby CL, Duhamel J-R (1991) Heterogeneity of extrastriate visual areas and multiple parietal areas in the macaque monkey. Neuropsychologia 29:517-537.
23. Colby CL, Miller EK (1986) Eye movement related responses of neurons in superior temporal polysensory area of macaque. Soc Neurosci Abstr 12:1184.
24. Colby CL, Gattass R, Olson CR, Gross, CG (1988) Topographical organization of cortical afferents to extrastriate visual area PO in the macaque: a dual tracer study. J Comp Neurol 269:392-413.
25. Colby CL, Duhamel J-R, Goldberg ME (1993) Ventral intraparietal area of the macaque: anatomic location and visual response properties. J Neurophysiol 69:902-914.
26. Dassonville P, Schlag J, Schlag-Rey M (1992) The frontal eye field provides the goal of saccadic eye movements. Exp Brain Res 89: 300-310.
27. De Lima AD, Voigt T, Morrison JH (1990) Morphology of the cells within the inferior temporal gyrus that project to the prefrontal cortex in the macaque monkey. J Comp Neurol 296:159-172.
28. Desimone R, Ungerleider L.G (1986) Multiple visual areas in the caudal superior temporal sulcus of the macaque. J Comp Neurol 248: 164-189.
29. Distler C, Boussaoud D, Desimone R, Ungerleider LG (1993) Cortical connections of inferior temporal area TEO in macaque monkeys. J Comp Neurol 334:125-150.
30. Duffy CJ, Wurtz RH (1991) Sensitivity of MST neurons to optic flow stimuli. I. A continuum of response selectivity to large-field stimuli. J Neurophysiol 65:1329-1345.
31. Erickson RG, Dow BM, Snyder AZ (1989) Representation of the fovea in the superior temporal sulcus of the macaque monkey. Exp Brain Res 78:90-112.
32. Felleman DJ, Van Essen DC (1991) Distributed hierarchical processing in the primate cerebral cortex. Cereb Cortex 1:1-47.
33. 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.
34. Galaburda AM, Pandya DN (1983) The intrinsic architectonic and connectional organization of the superior temporal region of the rhesus monkey. J Comp Neurol 221:169-184.
35. Gallyas F (1979) Silver staining of myelin by means of physical development. Neurol Res 1:203-209.
36. Gattass R, Gross CG (1981) Visual topography of striate projection zone (MT) in posterior superior temporal sulcus of the macaque. J Neurophysiol 46:621-638.
37. Gattas R, Sousa APB, Gross CG (1988) Visuotopic organization and extent of V3 and V4 of the macaque. J Neurosci 8:1831-1845.
38. 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 298:235-241.
39. Godaux E, Cheron G, Mettens P (1990) Ketamine induces failure of the oculomotor neural integrator in the cat. Neurosci Lett 116:162-167.
40. Huerta MF, Krubitzer LA, Kaas JH (1987) Frontal eye fields as defined by intracortical microstimulation in squirrel monkeys, owl monkeys and macaque monkeys. II. Cortical connections. J Comp Neurol 271: 473-492.
41. Kaufman L, Richards W (1969) Spontaneous fixation tendencies for visual forms. Percept Psychophys 5:85-88.
42. Keating CF, Keating EG (1993) Monkeys and mug shots: cues used by rhesus monkeys (Macaco mulatto) to recognize a human face. J Comp Psychol 107:131-139.
43. Koch C, Ullman S (1985) Shifts in selective visual attention: towards the underlying neural circuitry. Hum Neurobiol 4:219-227.
44. Komatsu H, Wurtz RH (1988) Relation of cortical areas MT and MST to pursuit eye movements. I. Localization and visual properties of neurons. J Neurophysiol 60:580-603.
45. Krubilzer LA, Kaas JH (1990) Cortical connections of MT in four species of primates: areal, modular and retinotopic patterns. Vis Neurosci 5:165-204.
46. Kurylo DD, Skavenski AA (1991) Eye movements elicited by electrical stimulation of area PG in the monkey. J Neurophysiol 65:1243-1253.
47. Leichnetz GR (1989) Inferior frontal eye field projections to the pursuit- related dorsolateral pontine nucleus and middle temporal area (MT) in the monkey. Vis Neurosci 3:171-180.
48. Leichnetz GR (1990) Preoccipital cortex receives a differential input from the frontal eye field and projects to the pretectal olivary nucleus and other visuomotor-related structures in the rhesus monkey. Vis Neurosci 5:123-133.
49. Leichnetz GR, Goldberg ME (1988) Higher centers concerned with eye movement and visual attention: cerebral cortex and thalamus. In: Neuroanatomy of the oculomotor system (Büttner-Evvever JA, ed), pp 365-429. New York: Elsevier.
50. Leinonen L, Hyvärinen J, Sovijärvi ARA (1980) Functional properties of neurons in the tempero-parietal association cortex of awake monkey. Exp Brain Res 39:203-215.
51. Maguire WM, Baizer JS (1984) Visuotopic organization of the prelunate gyrus in rhesus monkey. J Neurosci 4:1690-1704.
52. Maioli MG, Squatrito S, Galletti C, Battaglini PP, Sanserverino ER (1983) Corticocortical connections from the visual region of the superior temporal sulcus to frontal eye field in the macaque. Brain Res 265:294-299.
53. 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.
54. Maunsell JHR, Van Essen DC (1983) The connections of the middle temporal visual area (MT) and their relationship to a cortical hierarchy in the macaque monkey. J Neurosci 3:2563-2586.
55. Merigan WH, Maunsell JHR (1993) How parallel are the primate visual pathways? Annu Rev Neurosci 16:369-402.
56. Mohler CW, Goldberg ME, Wurtz RH (1973) Visual receptive fields of frontal eye field neurons. Brain Res 61:385-389.
57. Morel A, Bullier J (1987) Cortical connections of intraparietal and inferotemporal visual areas in the macaque monkey: a double-labeling study. Soc Neurosci Abstr 177:14.
58. Morel A, Bullier J (1990) Anatomical segregation of two cortical visual pathways in the macaque monkey. Vis Neurosci 4:555-578.
59. Morel A, Garraghty PE, Kaas JH (1993) Tonotopic organization, architectonic fields and connections of auditory cortex in macaque monkeys. J Comp Neurol 335:437-459.
60. Musil SY, Olson CR, Goldberg ME (1991) Posterior cingulate cortex of rhesus monkey: mechanisms of orbital-position and postsaccadic sensitivity. Soc Neurosci Abstr 17:442.
61. Musil SY, Olson CR, Goldberg ME (1992) Visual response properties of single neurons in posterior cingulate cortex of rhesus monkey. Soc Neurosci Abstr 18:148.
62. Newsome WT, Maunsell JHR, Van Essen DC (1986) The ventral posterior visual area of the macaque: visual topography and areal boundaries. J Comp Neurol 252:139-153.
63. Parthasarathy HB, Schall JD, Graybiel AM (1992) Distributed but convergent ordering of corticostriatal projections: analysis of the frontal eye field and the supplementary eye field in the macaque monkey. J Neurosci 12:4468-4488.
64. Perkel DH, Bullier J, Kennedy H (1986) Topography of the afferent connectivity of area 17 of the macaque monkey: a double-labeling study. J Comp Neurol 253:374-402.
65. Petrides M, Pandya DN (1984) Projections to the frontal cortex from the posterior parietal region in the rhesus monkey. J Comp Neurol 228:105-116.
66. Petrides M, Pandya DN (1988) Association fiber pathways to the frontal cortex from the superior temporal region in the rhesus monkey. J Comp Neurol 273:52-66.
67. Preuss TM, Goldman-Rakic PS (1991) Myelo- and cytoarchitecture of the granular frontal cortex and surrounding regions of the strepsirhine primate Galago and the anthropoid primate Macaca. J Comp Neurol 310:429-474.
68. Rayner K (1992) Eye movements and visual cognition: scene perception and reading. New York: Springer.
69. Robinson DA, Fuchs AF (1969) Eye movements evoked by stimulation of frontal eye fields. J Neurophysiol 32:637-648.
70. Royden CS, Banks MS, Crowell JA (1992) The perception of heading during eye movements. Nature 360:583-585.
71. Sakagami M, Niki H (1994) Encoding of behavioral significance of visual stimuli by primate prefrontal neurons: relation to relevant task conditions. Exp Brain Res 97:423-436.
72. Schall JD (1991a) Neuronal activity related to visually guided saccadic eye movements in the supplementary motor area of rhesus monkeys. J Neurophysiol 66:530-558.
73. Schall JD (1991b) Neuronal activity related to visually guided saccades in the frontal eye fields of rhesus monkeys: comparison with supple-mentary eye fields. J Neurophysiol 66:559-579.
74. Schall JD, Hanes DP (1993) Neural basis of saccade target selection in frontal eye field during visual search. Nature 366:467-469.
75. Schall JD, Morel A, King DJ, Whalley C (1991) Topography of connections between cortical visuomotor areas in the macaque. Soc Neurosci Abstr 17:857.
76. Schall JD, King DJ, Morel A (1993a) Topography of afferents to frontal eye field from superior temporal sulcus in macaque. Soc Neurosci Abstr 19.
77. Schall JD, Morel A, Kaas JH (1993b) Topography of supplementary eye field afferents to frontal eye field in macaque: implications for mapping between saccade coordinate systems. Vis Neurosci 10:385-393.
78. Schall JD, Hanes DP, Thompson KG (1995) Neural correlates of saccade target selection in macaque frontal eye field during visual search. J Neurosci (submitted).
79. Segraves MA (1992) Activity of monkey frontal eye field neurons projecting to oculomotor regions of the pons. J Neurophysiol 68:1967-1985.
80. Segraves MA, Goldberg ME (1987) Functional properties of corticotectal neurons in the monkey's frontal eye fields. J Neurophysiol 58: 1387-1419.
81. Seltzer B, Pandya DN (1978) Afferent cortical connections and architectonics of the superior temporal sulcus and surrounding cortex in the rhesus monkey. Brain Res 149:1-24.
82. Seltzer B, Pandya DN (1989) Frontal lobe connections of the superior temporal sulcus in the rhesus monkey. J Comp Neurol 281:97-113.
83. Spitzer H, Desimone R, Moran J (1988) Increased attention enhances both behavioral and neuronal performance. Science 240:338-340.
84. Stanton GB, Goldberg ME, Bruce CJ (1988) Frontal eye field efferents in the macaque monkey: I. subcortical pathways and topography of striatal and thalamic terminal fields. J Comp Neurol 271:473-492.
85. Stanton GB, Deng S-Y, Goldberg ME, McMullen NT (1989) Cytoarchitectural characteristics of the frontal eye fields in macaque monkeys. J Comp Neurol 282:415-427.
86. Stanton GB, Bruce CJ, Goldberg ME (1993) Topography of projections to the frontal lobe from the macaque frontal eye fields. J Comp Neurol 330:286-301.
87. Suzuki H, Azuma M (1983) Topographic studies on visual neurons BJ the dorsolateral prefrontal cortex of the monkey. Exp Brain Res 53: 47-58.
88. Tanaka K, Saito H-A, Fukada Y, Moriya M (1991) Coding visual images of objects in the inferotemporal cortex of the macaque monkey. J Neurophysiol 66:170-189.
89. Tanaka M, Lindsley E, Lausmann S, Creutzfeldt OD (1990) Afferent connections of the prelunate visual association cortex (areas V4 and DP). Anat Embryol 181:19-30.
90. Thier P, Andersen, RA (1991) Electrical microstimulation delineates 3 distinct eye-movement related areas in the posterior parietal cortex of the rhesus monkey. Soc Neurosci Abstr 17:1281.
91. Thompson KG, Hanes DP, Tu FF, Schall JD (1993) Evolution of saccade target selection signal in frontal eye field during visual search. Soc Neurosci Abstr 19:27.
92. Ungerleider LG, Desimone R (1986a) Projections to the superior temporal sulcus from the central and peripheral field representations of V1 and V2. J Comp Neurol 248:147-163.
93. Ungerleider LG, Desimone R (1986b) Cortical connections of visual area MT in the macaque. J Comp Neurol 248:190-222.
94. Ungerleider LG, Mishkin M (1982) Two cortical visual systems. In: Analysis of visual behavior (Ingle DJ, Goodale MA, Mansfield RJW, eds), PP 549-586. Cambridge, MA: MIT Press.
95. Ungerleider LG, Gaffan D, Pelak VS (1989) Projections from inferior temporal cortex to prefrontal cortex via the uncinate fascicle in rhesus monkeys. Exp Brain Res 76:473-484.
96. Vaadia E, Benson DA, Hienz RD, Goldstein MH (1986) Unit study of monkey frontal cortex: active localization of auditory and of visual stimuli. J Neurophysiol 56:934-952.
97. Van Essen DC, Maunsell JHR (1980) Two-dimensional maps of the cerebral cortex. J Comp Neurol 191:255-281.
98. Van Essen DC, Zeki SM (1978) The topographic organization of rhesus monkey prestriate cortex. J Physiol (Lond) 277:193-226.
99. Van Essen DC, Maunsell JHR, Bixby JL (1981) The middle temporal visual area in the macaque: myeloarchitecture, connections, functional properties and topography organization. J Comp Neurol 199:293-326.
100. Van Essen DC, Newsome WT, Maunsell JHR, Bixby JL (1986) The projections from striate cortex (V1) to areas V2 and V3 in the macaque monkey: asymmetries, areal boundaries and patchy connections. J Comp Neurol 224:451-480.
101. Viviani P (1990) Eye movements in visual search: cognitive, perceptual and motor control aspects. In: Eye movements and their role in visual and cognitive processes (Kowler E, ed), pp 353-393. New York: Elsevier.
102. von Bonin G, Bailey P (1947) The neocortex of Macaca mulatta. Urbana: University of Illinois.
103. Walker AE (1940) A cytoarchitectural study of the prefrontal area of the macaque monkey. J Comp Neurol 73:59-86.
104. Warren WH, Morris MW, Kalish M (1988) Perception of translational heading from optical flow. J Exp Psychol Hum Percept Perform 14: 646-660.
105. Weller RE, Kaas JH (1987) Subdivisions and connections of inferior temporal cortex in owl monkeys. J Comp Neurol 256:137-172.
106. Wilson FAW, Ó Scalaidhe SP, Goldman-Rakic PS (1993) Dissociation of object and spatial processing domains in primate prefrontal cortex. Science 260:1955-1958.
107. Yarbus AL (1967) Eye movements and vision. New York: Plenum.
108. Young MP (1992) Objective analysis of the topological organization of the primate cortical visual system. Nature 358:152-154.