Cortical connectivity suggests a role in limb coordination for macaque area PE of the superior parietal cortex

Journal of Neuroscience

Volumn 33, Issue 15, 2013, Pages 6648-6658

  Bakola, Sophia ^a,b   Passarelli, Lauretta ^a   Gamberini, Michela ^a   Fattori, Patrizia ^a   Galletti, Claudio ^a  

^a UNIVERSITY OF BOLOGNA   (Italy)

^b MONASH UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ERYTHROMYCIN; KETOROLAC; MANNITOL;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; FRONTAL CORTEX; HISTOLOGY; INTRAPARIETAL SULCUS; LIMB; MACACA FASCICULARIS; MALE; MICROSCOPY; MOTOR COORDINATION; NONHUMAN; PARIETAL CORTEX; PRIMARY MOTOR CORTEX; PRIORITY JOURNAL; SENSORY NERVE; SOMATOSENSORY CORTEX; SUPERIOR PARIETAL LOBULE;

ANIMALS; CELL MOVEMENT; CEREBRAL CORTEX; GYRUS CINGULI; MACACA FASCICULARIS; MALE; MICROINJECTIONS; MOTOR CORTEX; NEURAL PATHWAYS; NEUROANATOMICAL TRACT-TRACING TECHNIQUES; NEURONAL TRACT-TRACERS; PARIETAL LOBE;

EID: 84875974892     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4685-12.2013     Document Type: Article

References (92)

1. Abdollahi RO, Jastorff J, Orban GA (2012) Common and segregated processing of observed actions in human SPL. Cereb Cortex Advance online publication. Retrieved August 23, 2012. doi: 10.1093/cercor/bhs264.
2. Archambault PS, Caminiti R, Battaglia-Mayer A (2009) Cortical mechanisms for online control of hand movement trajectory: the role of the posterior parietal cortex. Cereb Cortex 19:2848-2864.
3. Archambault PS, Ferrari-Toniolo S, Battaglia-Mayer A (2011) Online control of hand trajectory and evolution of motor intention in the parieto-frontal system. J Neurosci 31:742-752.
4. Bakola S, Gamberini M, Passarelli L, Fattori P, Galletti C (2010) Cortical connections of parietal field PEc in the macaque: linking vision and somatic sensation for the control of limb action. Cereb Cortex 20:2592-2604.
5. 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.
6. Battaglia-Mayer A, Caminiti R, Lacquaniti F, Zago M (2003) Multiple levels of representation of reaching in the parieto-frontal network. Cereb Cortex 13:1009-1022.
7. Beloozerova IN, Sirota MG (2003) Integration of motor and visual information in the parietal area 5 during locomotion. J Neurophysiol 90:961-971.
8. Borra E, Belmalih A, Calzavara R, Gerbella M, Murata A, Rozzi S, Luppino G (2008) Cortical connections of the macaque anterior intraparietal (AIP) area. Cereb Cortex 18:1094-1111.
9. Bremner LR, Andersen RA (2012) Coding of the reach vectorinparietal area 5d. Neuron 75:342-351.
10. Breveglieri R, Galletti C, Gamberini M, Passarelli L, Fattori P (2006) So-matosensory cells in area PEc of macaque posterior parietal cortex. J Neurosci 26:3679-3684.
11. Brinkman C (1984) Supplementary motor area of the monkey's cerebral cortex: short- and long-term deficits after unilateral ablation and the effects of subsequent callosal section. J Neurosci 4:918-929.
12. Burbaud P, Doegle C, Gross C, Bioulac B (1991) A quantitative study of neuronal discharge in areas 5, 2, and 4 of the monkey during fast arm movements. J Neurophysiol 66:429-443.
13. Burman K, Palmer S, Gamberini M, Spitzer M, Rosa M (2008) Anatomical and physiological definition of the motor cortex of the marmoset monkey. J Comp Neurol 506:860-876.
14. Burman KJ, Reser DH, Yu HH, Rosa MG (2011) Cortical input to the frontal pole of the marmoset monkey. Cereb Cortex 21:1712-1737.
15. Burton H, Fabri M (1995) Ipsilateral intracortical connectionsof physiologically defined cutaneous representations in areas 3b and 1 of macaque monkeys: projections in the vicinity of the central sulcus. J Comp Neurol 355:508-538.
16. Caminiti R, Chafee MV, Battaglia-Mayer A, Averbeck BB, Crowe DA, Georgopoulos AP (2010) Understanding the parietal lobe syndrome from a neurophysiological and evolutionary perspective. Eur J Neurosci 31: 2320-2340.
17. Cavada C, Goldman-Rakic PS (1989a) Posterior parietal cortex in rhesus monkey: I. Parcellation of areas based on distinctive limbic and sensory corticocortical connections. J Comp Neurol 287:393-421.
18. Cavada C, Goldman-Rakic PS (1989b) 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.
19. Chen A, DeAngelis GC, Angelaki DE (2011) Convergence of vestibular and visual self-motion signals in an area of the posterior sylvian fissure. J Neurosci 31:11617-11627.
20. 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.
21. Culham JC, Cavina-Pratesi C, Singhal A (2006) The roleofparietal cortex in visuomotor control: what have we learned from neuroimaging? Neuro-psychologia 44:2668-2684.
22. Darian-Smith C, Darian-Smith I, Burman K, Ratcliffe N (1993) Ipsilateral cortical projections to areas 3a, 3b, and4 in the macaque monkey. J Comp Neurol 335:200-213.
23. Duffy FH, Burchfiel JL (1971) Somatosensory system: organizational hierarchy from single units in monkey area 5. Science 172:273-275.
24. Falchier A, Clavagnier S, Barone P, Kennedy H (2002) Anatomical evidence of multimodal integration in primate striate cortex. J Neurosci 22:5749-5759.
25. Ferraina S, Bianchi L (1994) Posterior parietal cortex: functional properties of neurons in area 5 during an instructed delay reaching task within different parts of space. Exp Brain Res 99:175-178.
26. Friedman DP, Jones EG, Burton H (1980) Representation pattern in the second somatic sensory area of the monkey cerebral cortex. J Comp Neurol 192:21-41.
27. Galletti C, Fattori P, Kutz DF, Gamberini M (1999) Brain location and visual topography of cortical area V6A in the macaque monkey. Eur J Neu-rosci 11:575-582.
28. Galletti C, Gamberini M, Kutz DF, Baldinotti I, Fattori P (2005) The relationship between V6 and PO in macaque extrastriate cortex. Eur J Neu-rosci 21:959-970.
29. Gallyas F (1979) Silver staining of myelin by means of physical development. Neurol Res 1:203-209.
30. Gamberini M, Passarelli L, Fattori P, Zucchelli M, Bakola S, Luppino G, Galletti C (2009) Cortical connections of the visuomotor parieto-occipital area V6Ad of the macaque monkey. J Comp Neurol 513:622-642.
31. Georgopoulos AP, Grillner S (1989) Visuomotor coordination in reaching and locomotion. Science 245:1209-1210.
32. Gerbella M, Belmalih A, Borra E, Rozzi S, Luppino G (2011) Cortical connections of the anterior (F5a) subdivision of the macaque ventral premo-tor area F5. Brain Struct Funct 216:43-65.
33. Geyer S, Matelli M, Luppino G, Zilles K (2000) Functional neuroanatomy of the primate isocortical motor system. Anat Embryol 202:443-474.
34. Ghosh S, Brinkman C, Porter R (1987) A quantitative study of the distribution of neurons projecting to the precentral motor cortex in the monkey (M. fascicularis). J Comp Neurol 259:424-444.
35. Graziano MS, Cooke DF, Taylor CS (2000) Coding the location of the arm by sight. Science 290:1782-1786.
36. Gregoriou GG, Borra E, Matelli M, Luppino G (2006) Architectonic organization of the inferior parietal convexity of the macaque monkey. J Comp Neurol 496:422-451.
37. Guldin WO, Grüsser OJ (1998) Is the reavestibular cortex? Trends Neurosci 21:254-259.
38. Hatanaka N, Nambu A, Yamashita A, Takada M, Tokuno H (2001) Soma-totopic arrangement and corticocortical inputs of the hindlimb region of the primary motor cortexin the macaque monkey. Neurosci Res 40:9-22.
39. Heed T, Beurze SM, Toni I, Röder B, Medendorp WP (2011) Functional rather than effector-specific organization of human posterior parietal cortex. J Neurosci 31:3066-3076.
40. Huffman KJ, Krubitzer L (2001) Area 3a: topographic organization and cortical connections in marmoset monkeys. Cereb Cortex 11:849-867.
41. Hutchins KD, Martino AM, Strick PL (1988) Corticospinal projections from the medial wall of the hemisphere. Exp Brain Res 71:667-672.
42. Hyvärinen J (1982) Posterior parietal lobe of the primate brain. Physiol Rev 62:1060-1129.
43. Johnson PB, Ferraina S, Bianchi L, Caminiti R (1996) Cortical networks for visual reaching: physiological and anatomical organization of frontal and parietal lobe arm regions. Cereb Cortex 6:102-119.
44. Jones EG, Coulter JD, Hendry SH (1978) Intracortical connectivityofarchi-tectonic fields in the somatic sensory, motor and parietal cortex of monkeys. J Comp Neurol 181:291-347.
45. Kalaska JF (1996) Parietal cortex area 5 and visuomotor behavior. Can J Physiol Pharmacol 74:483-498.
46. Krubitzer LA, Kaas JH (1990) The organization and connections of somato-sensory cortex in marmosets. J Neurosci 10:952-974.
47. Krubitzer L, Disbrow E (2008) The evolution of parietal areas involved in hand use in primates. In: The senses: a comprehensive reference (Kaas J, Gardner E, eds), pp 183-214. London: Elsevier.
48. Kurata K, Wise SP (1988) Premotor and supplementary motor cortex in rhesus monkeys: neuronal activity during externally- and internally-instructed motor tasks. Exp Brain Res 72:237-248.
49. Lacquaniti F, Guigon E, Bianchi L, Ferraina S, Caminiti R (1995) Representing spatial information for limb movement: role of area 5 in the monkey. Cereb Cortex 5:391-409.
50. Legendre P (2005) Species associations: the Kendall coefficient of concordance revisited. J Agric Biol Environ Stat 10:226-245.
51. Leichnetz GR (1986) Afferent and efferent connections of the dorsolateral precentral gyrus (area 4, hand/arm region) in the macaque monkey, with comparisons to area 8. J Comp Neurol 254:460-492.
52. Lewis JW, Van Essen DC (2000a) Mapping of architectonic subdivisions in the macaque monkey, with emphasis on parieto- occipital cortex. J Comp Neurol 428:79-111.
53. Lewis JW, Van Essen DC (2000b) Corticocortical connections of visual, sen-sorimotor, and multimodal processing area in the parietal lobe of the macaque monkey. J Comp Neurol 428:112-137.
54. Lewis JW, Burton H, Van Essen DC (1999) Anatomical evidence for the posterior boundary of area 2 in the macaque monkey. Somatosens Motor Res 10:382-390.
55. 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: intracortical microstimulation study in the macaque monkey. J Comp Neurol 311:463-482.
56. Luppino G, Matelli M, Camarda R, Rizzolatti G (1993) Coricocortical connections of area F3 (SMA-proper) and area F6 (pre-SMA)in the macaque monkey. J Comp Neurol 338:114-140.
57. Marconi B, Genovesio A, Battaglia-Mayer A, Ferraina S, Squatrito S, Molinari M, Lacquaniti L, Caminiti R (2001) Eye-hand coordination during reaching: I. Anatomical relationships between parietal and frontal cortex. Cereb Cortex 11:513-527.
58. Marigold DS, Drew T (2011) Contribution of cells in the posterior parietal cortex to the planning of visually guided locomotion in the cat: effects of temporary visual interruption. J Neurophysiol 105:2457-2470.
59. Markov NT, Misery P, Falchier A, Lamy C, Vezoli J, Quilodran R, Gariel MA, Giroud P, Ercsey-Ravasz M, Pilaz LJ, Huissoud C, Barone P, Dehay C, Toroczkai Z, Van Essen DC, Kennedy H, Knoblauch K (2011) Weight consistency specifies regularities of macaque cortical networks. Cereb Cortex 21:1254-1272.
60. 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.
61. Matelli M, Govoni P, Galletti C, Kutz DF, Luppino G (1998) Superior area 6 afferents from the superior parietal lobule in the macaque monkey. J Comp Neurol 402:327-352.
62. Mesulam MM, Rosene DL (1979) Sensitivity in horseradish peroxidase neurohistochemistry: a comparative and quantitative studyof nine methods. J Histochem Cytochem 27:763-773.
63. Morecraft RJ, Cipolloni PB, Stilwell-Morecraft KS, Gedney MT, Pandya DN (2004) Cytoarchitecture and cortical connections of the posterior cingu-late and adjacent somatosensory fields in the rhesus monkey. J Comp Neurol 469:37-69.
64. Mountcastle VB, Lynch JC, Georgopoulos A, Sakata H, Acuna C (1975) Posterior parietal association cortex of the monkey: command function for operations within extrapersonal space. J Neurophysiol 38:871-908.
65. Murray EA, Coulter JD (1981) Supplementary sensory area: the medial parietal cortex in the monkey. In: Cortical sensory organization (Woolsey CN, ed), pp 167-195. Clifton, NJ: Humana.
66. Padberg J, Franca JG, Cooke DF, Soares JG, Rosa MG, Fiorani M Jr, Gattass R, Krubitzer L (2007) Parallel evolution of cortical areas involved in skilled hand use. J Neurosci 27:10106-10115.
67. Palmer SM, Rosa MG (2006) Adistinct anatomical network of cortical areas for analysis of motion in far peripheral vision. Eur J Neurosci 24:2389-2405.
68. Pandya DN, Seltzer B (1982) Intrinsic connections and architectonics of posterior parietal cortex in the rhesus monkey. J Comp Neurol 204:196-210.
69. Passarelli L, Rosa MG, Gamberini M, Bakola S, Burman KJ, Fattori P, Galletti C (2011) Cortical connections of area V6Av in the macaque: a visual-input node to the eye/hand coordination system. J Neurosci 31:1790-1801.
70. Pearson RC, Powell TP (1978) The cortico-cortical connections to area 5 of the parietal lobe from the primary somatic sensory cortex of the monkey. Proc R Soc Lond B Biol Sci 200:103-108.
71. Petrides M, Pandya DN (1984) Projections to the frontal cortex from the posterior pariental region inthe rhesus monkey. JComp Neurol 228:105-116.
72. Pons TP, Kaas JH (1986) Corticocortical connections of area 2 of somato-sensory cortex in macaque monkeys: a correlative anatomical and electrophysiological study. J Comp Neurol 248:313-335.
73. Pons TP, Garraghty PE, Cusick CG, Kaas JH (1985) The somatotopic organization of area 2 in macaque monkeys. J Comp Neurol 241:445-466.
74. Reser DH, Burman KJ, Yu HH, Chaplin TA, Richardson KE, Worthy KH, Rosa MG (2012) Contrasting patterns of cortical input to architectural subdivisions of the area 8 complex: a retrograde tracing study in marmoset monkeys. Cereb Cortex Advance online publication. Retrieved June 26, 2012. doi: 10.1093/cercor/bhs177.
75. Robinson CJ, Burton H (1980) Organization of somatosensory receptive fields in cortical areas 7b, retroinsula, postauditory, and granular insula of M. fascicularis. J Comp Neurol 192:69-92.
76. Romo R, Schultz W (1987) Neuronal activity preceding self-initiated or externally timed arm movements in area 6 of monkey cortex. Exp Brain Res 67:656-662.
77. Rosa MG, Tweedale R (2005) Brain maps, great and small: lessons from comparative studies of primate visual cortical organization. Philos Trans R Soc Lond B Biol Sci 360:665-691.
78. Rosa MG, Palmer SM, Gamberini M, Tweedale R, Piñon MC, Bourne JA (2005) Resolving the organizationofthe New World monkey third visual complex: The dorsal extrastriate cortex of the marmoset (Callithrix jac-chus). J Comp Neurol 483:164-191.
79. Sakata H, Takaoka Y, Kawarasaki A, Shibutani H (1973) Somatosensory properties of neurons in superior parietal cortex (area 5) of the rhesus monkey. Brain Res 64:85-102.
80. Sato N, Sakata H, Tanaka YL, Taira M (2006) Navigation-associated medial parietal neurons in monkeys. Proc Natl Acad Sci U S A 103:17001-17006.
81. Sato N, Sakata H, Tanaka YL, Taira M (2010) Context-dependent place-selective responses of the neurons in the medial parietal region of macaque monkeys. Cereb Cortex 20:846-858.
82. Seal J, Gross C, Bioulac B (1982) Activity of neurons in area 5 during a simple arm movement in monkeys before and after deafferentation of the trained limb. Brain Res 250:229-243.
83. Sheskin D (2004) Handbook of parametric and nonparametric statistical procedures, Ed 3. Boca Raton, FL: Chapman and Hall/CRC.
84. Siegel S (1956) Nonparametric statistics for the behavioral sciences. New York: McGraw-Hill.
85. Snyder LH, Batista AP, Andersen RA (1998) Change in motor plan, without a change in the spatial locus of attention, modulates activity in posterior parietal cortex. J Neurophysiol 79:2814-2819.
86. Tanji J, Shima K (1994) Role for supplementary motor area cells in planning several movements ahead. Nature 371:413-416.
87. Taoka M, Toda T, Iwamura Y (1998) Representation of the midline trunk, bilateral arms, and shoulders in the monkey postcentral somatosensory cortex. Exp Brain Res 123:315-322.
88. Taoka M, Toda T, Iriki A, Tanaka M, Iwamura Y (2000) Bilateral receptive field neurons in the hindlimb region of the postcentral somatosensory cortex in awake macaque monkeys. Exp Brain Res 134:139-146.
89. Van Essen DC, Drury HA, Dickson J, Harwell J, Hanlon D, Anderson CH (2001) An integrated software suite for surface-based analyses of cerebral cortex. J Am Med Inform Assoc 8:443-459.
90. Vogt BA, Vogt L, Farber NB, Bush G (2005) Architecture and neurocytology of monkey cingulate gyrus. J Comp Neurol 485:218-239.
91. von Bonin G, Bailey P (1947) The neocortex of Macaca mulatta. Urbana, IL: University of Illinois.
92. Wall MB, Smith AT (2008) The representation of egomotion in the human brain. Curr Biol 18:191-194.