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Relationship between the corticostriatal terminals from areas 9 and 46, and those from area 8A, dorsal and rostral premotor cortex and area 24c: an anatomical substrate for cognition to action

Roberta Calzavara, Philippe Mailly, Suzanne N. Haber

European Journal of Neuroscience · 2007

doi:10.1111/j.1460-9568.2007.05825.x

Abstract

Our previous data indicate that there are specific features of the corticostriatal pathways from the prefrontal cortex. First, corticostriatal pathways are composed of focal, circumscribed projections and of diffuse, widespread projections. Second, there is some convergence between terminal fields from different functional regions of the prefrontal cortex. Third, anterior cingulate projections from area 24b occupy a large region of the rostral striatum. The goal of this study was to determine whether these features are also common to the corticostriatal projections from area 8A (including the frontal eye field; FEF), the supplementary eye field (SEF), dorsal and rostral premotor cortex (PMdr) and area 24c. Using a new approach of three‐dimensional reconstruction of the corticostriatal pathways, along with dual cortical tracer injections, we mapped the corticostriatal terminal fields from areas 9 and 46, 8A‐FEF, SEF, PMdr and 24b and c. In addition, we placed injections of retrogradely transported tracers into key striatal regions. The results demonstrated that: (i) a diffuse projection system is a common feature of the corticostriatal projections from different frontal regions; (ii) key striatal regions receive convergent projections from areas 9 and 46 and from areas 8A‐FEF, SEF, PMdr and 24c, suggesting a potential pivotal role of these striatal regions in integrating cortical information; (iii) projections from area 24c, like those from area 24b, terminate widely throughout the striatum, interfacing with terminals from several frontal areas. These features of the corticostriatal frontal pathways suggest a potential integrative striatal network for learning.

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References 76

  1. 1.

    Barbas H. Anatomic organization of basoventral and mediodorsal visual recipient prefrontal regions in the Rhesus monkey. J. Comp. Neurol. 1988;276:313-342.

    Not in our library10.1002/cne.902760302

  2. 2.

    Barbas H, Chauvel P, Delgado-Escueta AV. Architecture and cortical connections of the prefrontal cortex in the rhesus monkey. Advances in Neurology. 1992;91-115.

    Not in our library

  3. 3.

    Barbas H, Pandya DN. Architecture and frontal cortical connections of the premotor cortex (area 6) in the rhesus monkey. J. Comp. Neurol. 1987;256:211-228.

    Not in our library10.1002/cne.902560203

  4. 4.

    Boussaoud D. Attention versus intention in the primate premotor cortex. Neuroimage. 2001;14:S40-S45.

    Not in our library10.1006/nimg.2001.0816

  5. 5.

    Bouyer JJ, Park DH, Joh TH, Pickel VM. Chemical and structural analysis of the relation between cortical inputs and tyrosine hydroxylase-containing terminals in rat neostriatum. Brain Res. 1984;302:267-275.

    Not in our library10.1016/0006-8993(84)90239-7

  6. 6.

    Brasted PJ, Wise SP. Comparison of learning-related neuronal activity in the dorsal premotor cortex and striatum. Eur. J. Neurosci. 2004;19:721-740.

    Not in our library10.1111/j.0953-816x.2003.03181.x

  7. 7.

    Bruce CJ, Goldberg ME, Bushnell MC, Stanton GB. Primate frontal eye fields. II. Physiological and anatomical correlates of electrically evoked eye movements. J. Neurophysiol. 1985;54:714-734.

    Not in our library10.1152/jn.1985.54.3.714

  8. 8.

    Carmichael ST, Price JL. Connectional networks within the orbital and medial prefrontal cortex of Macaque monkeys. J. Comp. Neurol. 1996;371:179-207.

    Not in our library10.1002/(sici)1096-9861(19960722)371:2<179::aid-cne1>3.0.co;2-#

  9. 9.

    Constantinidis C, Franowicz MN, Goldman-Rakic PS. The sensory nature of mnemonic representation in the primate prefrontal cortex. Nat. Neurosci. 2001;4:311-316.

    Not in our library10.1038/85179

  10. 10.

    D'Esposito M, Aguirre GK, Zarahn E, Ballard D, Shin RK, Lease J. Functional MRI studies of spatial and nonspatial working memory. Cogn. Brain Res. 1998;7:1-13.

    Not in our library10.1016/s0926-6410(98)00004-4

  11. 11.

    Flaherty AW, Graybiel AM. Corticostriatal transformations in the primate somatosensory system. Projections from physiologically mapped body-part representations. J. Neurophysiol. 1991;66:1249-1263.

    Not in our library10.1152/jn.1991.66.4.1249

  12. 12.

    Frith CD, Frith U. The neural basis of mentalizing. Neuron. 2006;50:531-534.

    Not in our library10.1016/j.neuron.2006.05.001

  13. 13.

    Fujii N, Graybiel AM. Time-varying covariance of neural activities recorded in striatum and frontal cortex as monkeys perform sequential-saccade tasks. Proc. Natl Acad. Sci. USA. 2005;102:9032-9037.

    Not in our library10.1073/pnas.0503541102

  14. 14.

    Funahashi S, Bruce CJ, Goldman-Rakic PS. Mnemonic coding of visual space in the monkey's dorsolateral prefrontal cortex. J. Neurophysiol. 1989;61:331-349.

    Not in our library10.1152/jn.1989.61.2.331

  15. 15.

    Funahashi S, Chafee MV, Goldman-Rakic PS. Prefrontal neuronal activity in rhesus monkeys performing a delayed anti-saccade task. Nature. 1993;365:753-756.

    Not in our library10.1038/365753a0

  16. 16.

    Graybiel AM. The basal ganglia: learning new tricks and loving it. Curr. Opin. Neurobiol. 2005;15:638-644.

    Not in our library10.1016/j.conb.2005.10.006

  17. 17.

    Graybiel AM, Penney JB, Bloom FE, Bjorklund A, Hokfelt T. Chemical achitecture of the basal ganglia. Handbook of Chemcial Neuroanatomy. 1999;227-284.

    Not in our library

  18. 18.

    Haber SN, Fudge JL, McFarland NR. Striatonigrostriatal pathways in primates form an ascending spiral from the shell to the dorsolateral striatum. J. Neurosci. 2000;20:2369-2382.

    Not in our library10.1523/jneurosci.20-06-02369.2000

  19. 19.

    Haber SN, Kim KS, Mailly P, Calzavara R. Reward-related cortical inputs define a large striatal region in primates that interface with associative cortical inputs, providing a substrate for incentive-based learning. J. Neurosci. 2006;26:8368-8376.

    Not in our library10.1523/jneurosci.0271-06.2006

  20. 20.

    Haber SN, Lynd-Balta E, Mitchell SJ. The organization of the descending ventral pallidal projections in the monkey. J. Comp. Neurol. 1993;329:111-129.

    Not in our library10.1002/cne.903290108

  21. 21.

    Hikosaka O, Nakahara H, Rand MK, Sakai K, Lu X, Nakamura K, Miyachi S, Doya K. Parallel neural networks for learning sequential procedures [published erratum appears in Trends Neurosci. 1999 December; 22 (12): following 568]. Trends Neurosci. 1999;22:464-471.

    Not in our library10.1016/s0166-2236(99)01439-3

  22. 22.

    Huerta MF, Krubitzer LA, Kaas JH. Frontal eye field as defined by intracortical microstimulation in squirrel monkeys, owl monkeys, and macaque monkeys. II. Cortical connections. J. Comp. Neurol. 1987;265:332-361.

    Not in our library10.1002/cne.902650304

  23. 23.

    Guide for the Care and Use of Laboratory Animals. 1996.

    Not in our library

  24. 24.

    Ito S, Stuphorn V, Brown JW, Schall JD. Performance monitoring by the anterior cingulate cortex during saccade countermanding. Science. 2003;302:120-122.

    Not in our library10.1126/science.1087847

  25. 25.

    Jog MS, Kubota Y, Connolly CI, Hillegaart V, Graybiel AM. Building neural representations of habits. Science. 1999;286:1745-1749.

    Not in our library10.1126/science.286.5445.1745

  26. 26.

    Kremer JR, Mastronarde DN, McIntosh JR. Computer visualization of three-dimensional image data using IMOD. J. Struct. Biol. 1996;116:71-76.

    Not in our library10.1006/jsbi.1996.0013

  27. 27.

    Kurata K. Corticocortical inputs to the dorsal and ventral aspects of the premotor cortex of macaque monkeys. Neuroscience Res. 1991;12:263-280.

    Not in our library10.1016/0168-0102(91)90116-g

  28. 28.
  29. 29.

    Lehericy S, Benali H, Van de Moortele PF, Pelegrini-Issac M, Waechter T, Ugurbil K, Doyon J. Distinct basal ganglia territories are engaged in early and advanced motor sequence learning. Proc. Natl Acad. Sci. USA. 2005;102:12566-12571.

    Not in our library10.1073/pnas.0502762102

  30. 30.

    Lu M-T, Preston JB, Strick PL. Interconnections between the prefrontal cortex and the premotor areas in the frontal lobe. J. Comp. Neurol. 1994;341:375-392.

    Not in our library10.1002/cne.903410308

  31. 31.

    Luppino G, Matelli M, Camarda RM, Gallese V, Rizzolatti G. 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. 1991;311:463-482.

    Not in our library10.1002/cne.903110403

  32. 32.

    Luppino G, Rozzi S, Calzavara R, Matelli M. Prefrontal and agranular cingulate projections to the dorsal premotor areas F2 and F7 in the macaque monkey. Eur. J. Neurosci. 2003;17:559-578.

    Not in our library10.1046/j.1460-9568.2003.02476.x

  33. 33.

    MacAvoy MG, Gottlieb JP, Bruce CJ. Smooth-pursuit eye movement representation in the primate frontal eye field. Cereb. Cortex. 1991;1:95-102.

    Not in our library10.1093/cercor/1.1.95

  34. 34.

    Matelli M, Luppino G, Rizzolatti G. Patterns of cytochrome oxidase activity in the frontal agranular cortex of the macaque monkey. Behav. Brain Res. 1985;18:125-136.

    Not in our library10.1016/0166-4328(85)90068-3

  35. 35.

    Matelli M, Luppino G, Rizzolatti G. Architecture of superior and mesial area 6 and the adjacent cingulate cortex in the macaque monkey. J. Comp. Neurol. 1991;311:445-462.

    Not in our library10.1002/cne.903110402

  36. 36.

    McFarland NR, Haber SN. Convergent inputs from thalamic motor nuclei and frontal cortical areas to the dorsal striatum in the primate. J. Neurosci. 2000;20:3798-3813.

    Not in our library10.1523/jneurosci.20-10-03798.2000

  37. 37.

    Middleton FA, Strick PL. Basal-ganglia ‘projections’ to the prefrontal cortex of the primate. Cereb. Cortex. 2002;12:926-935.

    Not in our library10.1093/cercor/12.9.926

  38. 38.

    Miller EK. The prefrontal cortex: complex neural properties for complex behavior. Neuron. 1999;22:15-17.

    Not in our library10.1016/s0896-6273(00)80673-x

  39. 39.

    Mitchell JP, Macrae CN, Banaji MR. Dissociable medial prefrontal contributions to judgments of similar and dissimilar others. Neuron. 2006;50:655-663.

    Not in our library10.1016/j.neuron.2006.03.040

  40. 40.

    Monchi O, Petrides M, Strafella AP, Worsley KJ, Doyon J. Functional role of the basal ganglia in the planning and execution of actions. Ann. Neurol. 2006;59:257-264.

    Not in our library10.1002/ana.20742

  41. 41.

    Nambu A, Kaneda K, Tokuno H, Takada M. Organization of corticostriatal motor inputs in monkey putamen. J. Neurophysiol. 2002;88:1830-1842.

    Not in our library10.1152/jn.2002.88.4.1830

  42. 42.

    O'Doherty J, Critchley H, Deichmann R, Dolan RJ. Dissociating valence of outcome from behavioral control in human orbital and ventral prefrontal cortices. J. Neurosci. 2003;23:7931-7939.

    Not in our library10.1523/jneurosci.23-21-07931.2003

  43. 43.

    Parthasarathy HB, Schall JD, Graybiel AM. Distributed but convergent ordering of corticostriatal projections: analysis of the frontal eye field and the supplementary eye field in the macaque monkey. J. Neurosci. 1992;12:4468-4488.

    Not in our library10.1523/jneurosci.12-11-04468.1992

  44. 44.

    Pasupathy A, Miller EK. Different time courses of learning-related activity in the prefrontal cortex and striatum. Nature. 2005;433:873-876.

    Not in our library10.1038/nature03287

  45. 45.

    Paus T. Primate anterior cingulate cortex: where motor control, drive and cognition interface. Nat. Rev. Neurosci. 2001;2:417-424.

    Not in our library10.1038/35077500

  46. 46.

    Paxinos G, Huang XF, Toga AW. The Rhesus Monkey in Stereotaxic Coordinates. 2000.

    Not in our library

  47. 47.

    di Pellegrino G, Wise SP. Visuospatial versus visuomotor activity in the premotor and prefrontal cortex of a primate. J. Neurosci. 1993;13:1227-1243.

    Not in our library10.1523/jneurosci.13-03-01227.1993

  48. 48.

    Petrides M. The role of the mid-dorsolateral prefrontal cortex in working memory. Exp. Brain Res. 2000;133:44-54.

    Not in our library10.1007/s002210000399

  49. 49.

    Petrides M, Alivisatos B, Evans AC, Meyer E. Dissociation of human mid-dorsolateral from posterior dorsolateral frontal cortex in memory processing. Proc. Natl Acad. Sci. USA. 1993;90:873-877.

    Not in our library10.1073/pnas.90.3.873

  50. 50.

    Petrides M, Alivisatos B, Frey S. Differential activation of the human orbital, mid-ventrolateral, and mid-dorsolateral prefrontal cortex during the processing of visual stimuli. Proc. Natl Acad. Sci. USA. 2002;99:5649-5654.

    Not in our library10.1073/pnas.072092299

  51. 51.

    Petrides M, Pandya DN. Dorsolateral prefrontal cortex: comparative cytoarchitectonic analysis in the human and the macaque brain and corticocortical connection patterns. Eur. J. Neurosci. 1999;11:1011-1036.

    Not in our library10.1046/j.1460-9568.1999.00518.x

  52. 52.

    Picard N, Strick PL. Imaging the premotor areas. Curr. Opin. Neurobiol. 2001;11:663-672.

    Not in our library10.1016/s0959-4388(01)00266-5

  53. 53.

    Ramanathan S, Hanley JJ, Deniau JM, Bolam JP. Synaptic convergence of motor and somatosensory cortical afferents onto GABAergic interneurons in the rat striatum. J. Neurosci. 2002;22:8158-8169.

    Not in our library10.1523/jneurosci.22-18-08158.2002

  54. 54.

    Redgrave P, Gurney K. The short-latency dopamine signal: a role in discovering novel actions? Nat. Rev. Neurosci. 2006;7:967-975.

    Not in our library10.1038/nrn2022

  55. 55.

    Rizzolatti G, Luppino G. The cortical motor system. Neuron. 2001;31:889-901.

    Not in our library10.1016/s0896-6273(01)00423-8

  56. 56.

    Rizzolatti G, Luppino G, Matelli M. The organization of the cortical motor system: new concepts. Electroencephalogr. Clin. Neurophysiol. 1998;106:283-296.

    Not in our library10.1016/s0013-4694(98)00022-4

  57. 57.

    Robinson DA, Fuchs AF. Eye movements evoked by stimulation of frontal eye fields. J. Neurophysiol. 1969;32:637-648.

    Not in our library10.1152/jn.1969.32.5.637

  58. 58.

    Roesch MR, Olson CR. Neuronal activity related to reward value and motivation in primate frontal cortex. Science. 2004;304:307-310.

    Not in our library10.1126/science.1093223

  59. 59.

    Rowe JB, Passingham RE. Working memory for location and time: activity in prefrontal area 46 relates to selection rather than maintenance in memory. Neuroimage. 2001;14:77-86.

    Not in our library10.1006/nimg.2001.0784

  60. 60.

    Rowe JB, Stephan KE, Friston K, Frackowiak RS, Passingham RE. The prefrontal cortex shows context-specific changes in effective connectivity to motor or visual cortex during the selection of action or colour. Cereb. Cortex. 2005;15:85-95.

    Not in our library10.1093/cercor/bhh111

  61. 61.

    Rowe JB, Toni I, Josephs O, Frackowiak RS, Passingham RE. The prefrontal cortex: response selection or maintenance within working memory? Science. 2000;288:1656-1660.

    Not in our library10.1126/science.288.5471.1656

  62. 62.

    Schlag J, Schlag-Rey M. Evidence for a supplementary eye field. J. Neurophysiol. 1987;57:179-200.

    Not in our library10.1152/jn.1987.57.1.179

  63. 63.

    Schultz W. Getting formal with dopamine and reward. Neuron. 2002;36:241-263.

    Not in our library10.1016/s0896-6273(02)00967-4

  64. 64.

    Selemon LD, Goldman-Rakic PS. Longitudinal topography and interdigitation of corticostriatal projections in the rhesus monkey. J. Neurosci. 1985;5:776-794.

    Not in our library10.1523/jneurosci.05-03-00776.1985

  65. 65.

    Simon SR, Meunier M, Piettre L, Berardi AM, Segebarth CM, Boussaoud D. Spatial attention and memory versus motor preparation: premotor cortex involvement as revealed by fMRI. J. Neurophysiol. 2002;88:2047-2057.

    Not in our library10.1152/jn.2002.88.4.2047

  66. 66.

    Stuphorn V, Taylor TL, Schall JD. Performance monitoring by the supplementary eye field. Nature. 2000;408:857-860.

    Not in our library10.1038/35048576

  67. 67.

    Takada M, Nambu A, Hatanaka N, Tachibana Y, Miyachi S, Taira M, Inase M. Organization of prefrontal outflow toward frontal motor-related areas in macaque monkeys. Eur. J. Neurosci. 2004;19:3328-3342.

    Not in our library10.1111/j.0953-816x.2004.03425.x

  68. 68.

    Takada M, Tokuno H, Nambu A, Inase M. Corticostriatal projections from the somatic motor areas of the frontal cortex in the macaque monkey: segregation versus overlap of input zones from the primary motor cortex, the supplementary motor area, and the premotor cortex. Exp. Brain Res. 1998;120:114-128.

    Not in our library10.1007/s002210050384

  69. 69.

    Toni I, Ramnani N, Josephs O, Ashburner J, Passingham RE. Learning arbitrary visuomotor associations: temporal dynamic of brain activity. Neuroimage. 2001;14:1048-1057.

    Not in our library10.1006/nimg.2001.0894

  70. 70.

    Toni I, Rowe J, Stephan KE, Passingham RE. Changes of cortico-striatal effective connectivity during visuomotor learning. Cereb. Cortex. 2002;12:1040-1047.

    Not in our library10.1093/cercor/12.10.1040

  71. 71.

    Walker AE. A cytoarchitectural study of the prefronal area of the macaque monkey. J. Comp. Neurol. 1940;73:59-86.

    Not in our library

  72. 72.

    Wallis JD, Anderson KC, Miller EK. Single neurons in prefrontal cortex encode abstract rules. Nature. 2001;411:953-956.

    Not in our library10.1038/35082081

  73. 73.

    Wallis JD, Miller EK. Neuronal activity in primate dorsolateral and orbital prefrontal cortex during performance of a reward preference task. Eur. J. Neurosci. 2003;18:2069-2081.

    Not in our library10.1046/j.1460-9568.2003.02922.x

  74. 74.

    Wilson CJ, Shepherd GM. The basal ganglia. Synaptic Organization of the Brain. 2004;361-413.

    Not in our library

  75. 75.

    Yeterian EH, Pandya DN. Prefrontostriatal connections in relation to cortical architectonic organization in Rhesus monkeys. J. Comp. Neurol. 1991;312:43-67.

    Not in our library10.1002/cne.903120105

  76. 76.

    Yeterian EH, Van Hoesen GW. Cortico-striate projections in the rhesus monkey: the organization of certain cortico-caudate connections. Brain Res. 1978;139:43-63.

    Not in our library10.1016/0006-8993(78)90059-8

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