Cortical and thalamic projections to cytoarchitectural areas 6Va and 8C of the marmoset monkey: Connectionally distinct subdivisions of the lateral premotor cortex

Journal of Comparative Neurology

Volumn 523, Issue 8, 2015, Pages 1222-1247

  Burman, Kathleen J ^a   Bakola, Sophia ^a   Richardson, Karyn E ^a   Yu, Hsin Hao ^a   Reser, David H ^a   Rosa, Marcello G P ^a  

^a MONASH UNIVERSITY   (Australia)

Author keywords

Connectivity; Evolution; Frontal cortex; Marmoset; Motor control

Indexed keywords

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; BRAIN FUNCTION; BRAIN REGION; CALLITRICHINAE; CONTROLLED STUDY; CYTOARCHITECTURE; EXTRASTRIATE BODY AREA; FEMALE; FRONTAL CORTEX; MALE; NEUROANATOMY; NONHUMAN; OCULOMOTOR SYSTEM; POSTERIOR PARIETAL CORTEX; PREMOTOR CORTEX; PRIMARY MOTOR CORTEX; PRIORITY JOURNAL; SECONDARY SOMATOSENSORY CORTEX; SENSORY NERVE; SIMIAN; THALAMUS NUCLEUS; VENTRAL PREMOTOR AREA; VISUAL INFORMATION; VISUOMOTOR COORDINATION; ANATOMY AND HISTOLOGY; ANIMAL; CALLITHRIX; CHEMISTRY; CYTOLOGY; NERVE CELL; NERVE TRACT; NEUROANATOMICAL TRACT TRACING; THALAMUS;

FLUORESCENT DYE; NEURONAL TRACT TRACER;

ANIMALS; CALLITHRIX; CEREBRAL CORTEX; FEMALE; FLUORESCENT DYES; MALE; NEURAL PATHWAYS; NEUROANATOMICAL TRACT-TRACING TECHNIQUES; NEURONAL TRACT-TRACERS; NEURONS; THALAMUS;

EID: 84926421372     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.23734     Document Type: Article

References (103)

1. 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.
2. Baker JT, Patel GH, Corbetta M, Snyder LH. 2006. Distribution of activity across the monkey cerebral cortical surface, thalamus and midbrain during rapid, visually guided saccades. Cereb Cortex 16:447-459.
3. Barbas H. 1988. Anatomic organization of basoventral and mediodorsal visual recipient prefrontal regions in the rhesus monkey. J Comp Neurol 276:313-342.
4. 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.
5. Blum B, Kulikowski JJ, Carden D, Harwood D. 1982. Eye movements induced by electrical stimulation of the frontal eye fields of marmosets and squirrel monkeys. Brain Behav Evol 21:34-41.
6. Burish MJ, Stepniewska I, Kaas JH. 2008. Microstimulation and architectonics of frontoparietal cortex in common marmosets (Callithrix jacchus). J Comp Neurol 507:1151-1168.
7. Burman KJ, Rosa MGP. 2009. Architectural subdivisions of medial and orbital frontal cortices in the marmoset monkey (Callithrix jacchus). J Comp Neurol 514:11-29.
8. Burman KJ, Palmer SM, Gamberini M, Rosa MGP. 2006. Cytoarchitectonic subdivisions of the dorsolateral frontal cortex of the marmoset monkey (Callithrix jacchus), and their projections to dorsal visual areas. J Comp Neurol 495:149-172.
9. Burman KJ, Palmer SM, Gamberini M, Spitzer MW, Rosa MGP. 2008. Anatomical and physiological definition of the motor cortex of the marmoset monkey. J Comp Neurol 506:860-876.
10. Burman KJ, Reser DH, Yu HH, Rosa MGP. 2011a. Cortical input to the frontal pole of the marmoset monkey. Cereb Cortex 21:1712-1737.
11. Burman KJ, Reser DH, Richardson KE, Gaulke H, Worthy KH, Rosa MGP. 2011b. Subcortical projections to the frontal pole in the marmoset monkey. Eur J Neurosci 34:303-319.
12. Burman KJ, Bakola, S, Richardson, KE, Reser DH, Rosa MGP. 2014a. Patterns of cortical input to the primary motor cortex in the marmoset monkey. J Comp Neurol 522:811-843.
13. Burman KJ, Bakola, S, Richardson, KE, Reser DH, Rosa MGP. 2014b. Patterns of cortical input to the caudal and rostral areas of the dorsal premotor cortex (6DC and 6DR) in the marmoset monkey. J Comp Neurol 522:3683-3716.
14. Carmichael ST, Price JL. 1995. Sensory and premotor connections of the orbital and medial prefrontal cortex of macaque monkeys. J Comp Neurol 363:642-664.
15. Changizi MA, Shimojo S. 2005. Parcellation and area-area connectivity as a function of neocortex size. Brain Behav Evol 66:88-98.
16. Chaplin TA, Yu H-H, Rosa MGP. 2013. Representation of the visual field in the primary visual area of the marmoset monkey: magnification factors, point-image size, and proportionality to retinal ganglion cell density. J Comp Neurol 521:1001-1019.
17. Deacon TW. 1992. Cortical connections of the inferior arcuate sulcus cortex in the macaque brain. Brain Res 573:8-26.
18. de Hoon MJL, Imoto S, Nolan J, Miyano S. 2004. Open Source Clustering Software. Bioinformatics 20:1453-1454.
19. de la Mothe LA, Blumell S, Kajikawa Y, Hackett TA. 2006. Cortical connections of the auditory cortex in marmoset monkeys: core and medial belt regions. J Comp Neurol 496:27-71.
20. Dancause N, Barbay S, Frost SB, Plautz EJ, Popescu M, Dixon PM, Stowe AM, Friel KM, Nudo RJ. 2006a. Topographically divergent and convergent connectivity between premotor and primary motor cortex. Cereb Cortex 16:1057-1068.
21. Dancause N, Barbay S, Frost SB, Plautz EJ, Stowe AM, Friel KM, Nudo RJ. 2006b. Ipsilateral connections of the ventral premotor cortex in a new world primate. J Comp Neurol 495:374-390.
22. Dum RP, Strick PL. 2002. Motor areas in the frontal lobe of the primate. Physiol Behav 77:677-682.
23. Dum RP, Strick PL. 2005. Frontal lobe inputs to the digit representations of the motor areas on the lateral surface of the hemisphere. J Neurosci 25:1375-1386.
24. Ferrari PF, Gallese V, Rizzolatti G, Fogassi L. 2003. Mirror neurons responding to the observation of ingestive and communicative mouth actions in the monkey ventral premotor cortex. Eur J Neurosci 17:1703-1714.
25. Fitzgerald PJ, Lane JW, Thakur PH, Hsiao SS. 2006a. Receptive fields properties of the macaque second somatosensory cortex: representation of orientation on different finger pads. J Neurosci 26:6473-6484.
26. Fitzgerald PJ, Lane JW, Thakur PH, Hsiao SS. 2006b. Receptive fields properties of the macaque second somatosensory cortex: RF size, shape and somatotopic organization. J Neurosci 26:6485-6495.
27. Fouad K, Klusman I, Schwab ME. 2004. Regenerating corticospinal fibers in the marmoset (Callithrix jacchus) after spinal cord lesion and treatment with the anti-Nogo-A antibody IN-1. Eur J Neurosci 20:2479-82.
28. Freret T, Bouet V, Toutain J, Saulnier R, Pro-Sistiaga P, Bihel E, Mackenzie ET, Roussel S, Schumann-Bard P, Touzani O. 2008. Intraluminal thread model of focal stroke in the non-human primate. J Cereb Blood Flow Metab 28:786-96.
29. Friedman DP, Murray EA, O'Neill JB, Mishkin M. 1986. Cortical connections of the somatosensory fields of the lateral sulcus of macaques: evidence for a corticolimbic pathway for touch. J Comp Neurol 252:323-347.
30. Fukushima K, Sato T, Fukushima J, Shinmei Y, Kaneko CRS. 2000. Activity of smooth pursuit-related neurons in the monkey periarcuate cortex during pursuit and passive whole-body rotation. J Neurophysiol 83:563-587.
31. Gallyas F. 1979. Silver staining of myelin by means of physical development. Neurol Res 1:203-209.
32. Gharbawie OA, Stepniewska I, Qi H, Kaas JH. 2011a. Multiple parietal-frontal pathways mediate grasping in macaque monkeys. J Neurosci 31:11660-11677.
33. Gharbawie OA, Stepniewska I, Kaas JH. 2011b. Cortical connections of functional zones in posterior parietal cortex and frontal cortex motor regions in New World monkeys. Cereb Cortex 21:1981-2002.
34. 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.
35. Gottlieb JP, MacAvoy MG, Bruce CJ. 1994. Neural responses related to smooth-pursuit eye movements and their correspondence with electrically elicited smooth eye movements in the primate frontal eye field. J Neurophysiol 72:1634-1653.
36. Graziano MS, Gandhi S. 2000. Location of the polysensory zone in the precentral gyrus of anesthetized monkeys. Exp Brain Res 135:259-266.
37. Hinkley LB, Krubitzer LA, Nagarajan SS, Disbrow EA. 2007. Sensorimotor integration in S2, PV, and parietal rostroventral areas of the human sylvian fissure. J Neurophysiol 97:1288-1297.
38. Huerta MF, Krubitzer LA, Kaas JH. 1987. Frontal eye field as defined by intracortical microstimulation in squirrel monkeys, owl monkeys, and macaque monkeys. II. Cortical connections. J Comp Neurol 265:332-361.
39. Huffman KJ, Krubitzer L. 2001. Area 3a: topographic organization and cortical connections in marmoset monkeys. Cereb Cortex 11:849-867.
40. Hunnicutt BJ, Long BR, Kusefoglu D, Gertz KJ, Zhong H, Mao T. 2014. A comprehensive thalamocortical projection map at the mesoscopic level. Nat Neurosci 17:1276-1285.
41. Ilinski IA, Kultas-Ilinski K. 1987. Sagittal cytoarchitectonic maps of the Macaca mulatta thalamus with a revised nomenclature of the motor-related nuclei validated by observations on their connectivity. J Comp Neurol 261:331-364.
42. Iyengar S, Qi HX, Jain N, Kaas JH. 2007. Cortical and thalamic connections of the representations of the teeth and tongue in somatosensory cortex of new world monkeys. J Comp Neurol 501:95-120.
43. Konomi T, Fujiyoshi K, Hikishima K, Komaki Y, Tsuji O, Okano HJ, Toyama Y, Okano H, Nakamura M. 2012. Conditions for quantitative evaluation of injured spinal cord by in vivo diffusion tensor imaging and tractography: preclinical longitudinal study in common marmosets. Neuroimage 63:1841-53.
44. Krubitzer LA, Kaas JH. 1990. The organization and connections of somatosensory cortex in marmosets. J Neurosci 10:952-974.
45. Kurata K. 1991. Corticocortical inputs to the dorsal and ventral aspects of the premotor cortex of macaque monkeys. Neurosci Res 12:263-280.
46. Legendre P. 2005. Species associations: the Kendall coefficient of concordance revisited. J Agric Biol Environ Stat 10:226-245.
47. Lewis JW, Van Essen DC. 2000. Corticocortical connections of visual, sensorimotor, and multimodal processing areas in the parietal lobe of the macaque monkey. J Comp Neurol 428:112-137.
48. Lu MT, Preston JB, Strick PL. 1994. Interconnections between the prefrontal cortex and the motor areas in the frontal lobe. J Comp Neurol 341:375-392.
49. Luppino G, Murata A, Govoni P, Matelli M. 1999. Largely segregated parietofrontal connections linking rostral intraparietal cortex (areas AIP and VIP) and the ventral premotor cortex (areas F4 and F5). Exp Brain Res 128:181-187.
50. Luppino G, Calzavara R, Rozzi S, Matelli M. 2001. Projections from the superior temporal sulcus to the agranular frontal cortex in the macaque. Eur J Neurosci 14:1035-1040.
51. Maggi P, Cummings Macri SM, Gaitán MI, Leibovitch E, Wholer JE, Knight HL, Ellis M, Wu T, Silva AC, Massacesi L, Jacobson S, Westmoreland S, Reich DS. 2014. The formation of inflammatory demyelinated lesions in cerebral white matter. Ann Neurol 76:594-608.
52. Maranesi M, Rodà F, Bononi L, Rozzi S, Ferrari PF, Fogassi L, Coudé G. 2012. Anatomo-functional organization of the ventral primary motor and premotor cortex in the macaque monkey. Eur J Neurosci 36:3376-3387.
53. Markov NT, Ercsey-Ravasz M, Lamy C, Ribieiro Gomes AR, Magrou L, Misery P, Giroud P, Barone P, Dehay C, Toroczkai Z, Knoblauch K, Van Essen DC, Kennedy H. 2013. The role of long-range connections on the specificity of the macaque interareal cortical network. Proc Natl Acad Sci U S A 110:5187-92.
54. Markov NT, Ercsey-Ravasz MM, Ribeiro Gomes AR, Lamy C, Magrou L, Vezoli J, Misery P, Falchier A, Quilodran R, Gariel MA, Sallet J, Gamanut R, Huissoud C, Clavagnier S, Giroud P, Sappey-Marinier D, Barone P, Dehay C, Toroczkai Z, Knoblauch K, Van Essen DC, Kennedy H. 2014. A weighted and directed interareal connectivity matrix for macaque cerebral cortex. Cereb Cortex 24:17-36.
55. Marshall JW, Ridley RM. 2003. Assessment of cognitive and motor deficits in a marmoset model of stroke. ILAR J 44:153-60.
56. Matelli M, Luppino G. 2001. Parietofrontal circuits for action and space perception in the macaque monkey. Neuroimage 14:S27-32.
57. 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.
58. Matelli M, Camarda R, Glickstein M, Rizzolatti G. 1986. Afferent and efferent projections of the inferior area 6 in the macaque monkey. J Comp Neurol 251:281-298.
59. Moschovakis AK, Gregoriou GG, Ugolini G, Doldan M, Graf W, Guldin W, Hadji Dimitrakis K, Savaki HE. 2004. Oculomotor areas of the primate frontal lobes: a transneuronal transfer of rabies virus and [14C]-2-deoxyglucose functional imaging study. J Neurosci 24:5726-5740.
60. Olszewski J. 1952. The thalamus of the Macaca mulatta: an atlas for use with the stereotaxic instrument. Basel: Karger.
61. Padberg J, Franca JG, Cooke DF, Soares JG, Rosa MGP, Fiorani M Jr, Gattass R, Krubitzer L. 2007. Parallel evolution of cortical areas involved in skilled hand use. J Neurosci 27:10106-10115.
62. Palmer SM, Rosa MGP. 2006a. Quantitative analysis of the corticocortical projections to the middle temporal area in the marmoset monkey: evolutionary and functional implications. Cereb Cortex 16:1361-1375.
63. Palmer SM, Rosa MGP. 2006b. A distinct anatomical network of cortical areas for analysis of motion in far peripheral vision. Eur J Neurosci 24:2389-2405.
64. Paxinos G, Watson C, Petrides M, Rosa M, Tokuno H. 2012. The marmoset brain in stereotaxic coordinates. London: Academic Press, Elsevier.
65. Petrides M, Pandya DN. 1999. Dorsolateral prefrontal cortex: comparative cytoarchitectonic analysis in the human and the macaque brain and corticocortical connection patterns. Eur J Neurosci 11:1011-1036.
66. Petrides M, Pandya DN. 2002. Comparative cytoarchitectonic analysis of the human and the macaque ventrolateral prefrontal cortex and corticocortical connection patterns in the monkey. Eur J Neurosci 16:291-310.
67. Pohlmeyer EA, Mahmoudi B, Geng S, Prins N, Sanchez JC. 2012. Brain-machine interface control of a robot arm using actor-critic rainforcement learning. Conf Proc IEEE Eng Med Biol Soc 2012:4108-4111.
68. Pohlmeyer EA, Mahmoudi B, Geng S, Prins NW, Sanchez JC. 2014. Using reinforcement learning to provide stable brain-machine interface control despite neural input reorganization. PLoS One 9:e87253.
69. Preuss TM, Goldman-Rakic. 1991.
70. Preuss TM, Stepniewska I, Kaas JH. 1996. Movement representation in the dorsal and ventral premotor areas of owl monkeys: a microstimulation study. J Comp Neurol 371:649-676.
71. Qi H-X, Lyon DC, Kaas JH. 2002. Cortical and thalamic connections of the parietal somatosensory area in marmoset monkeys (Callithrix jacchus). J Comp Neurol 443:168-182.
72. Raos V, Franchi G, Gallese V, Fogassi L. 2003. Somatotopic organization of the lateral part of area F2 (dorsal premotor cortex) of the macaque monkey. J Neurophysiol 89:1503-1518.
73. Reser DH, Burman KJ, Richardson KE, Spitzer MW, Rosa MGP. 2009. Connections of the marmoset rostrotemporal auditory area: express pathways for analysis of affective content in hearing. Eur J Neurosci 30:578-592.
74. Reser DH, Burman KJ, Yu HH, Chaplin TA, Richardson KE, Worthy KH, Rosa MGP. 2013. Contrasting patterns of cortical input to architectural subdivisions of the area 8 complex: a retrograde tracing study in marmoset monkeys. Cereb Cortex 23:1901-1922.
75. Rizzolatti G, Luppino G. 2001. The cortical motor system. Neuron 31:889-901.
76. Rizzolatti G, Luppino G, Matelli M. 1998. The organization of the cortical motor system: new concepts. Electroencephalogr Clin Neurophysiol 106:283-296.
77. Rizzolatti G, Fogassi L, Gallese V. 2002. Motor and cognitive functions of the ventral premotor cortex. Curr Opin Neurobiol 12:149-154.
78. Rizzolatti G, Cattaneo L, Fabbri-Destro M, Rozzi S. 2014. Cortical mechanisms underlying the organization of goal-directed actions and mirror neuron-based action understanding. Physiol Rev 94:655-706.
79. Rosa MGP. 2002. Visual maps in the adult primate cerebral cortex: some implications for brain development and evolution. Braz J Med Biol Res 35:1485-1498.
80. Rosa MGP, 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.
81. Rosa MGP, Soares JG, Fiorani M Jr, Gattass R. 1993. Cortical afferents of visual area MT in the Cebus monkey: possible homologies between New and Old World monkeys. Vis Neurosci 10:827-855.
82. Rosa MGP, Palmer SM, Gamberini M, Burman KJ, Yu HH, Reser DH, Bourne JA, Tweedale R, Galletti C. 2009. Connections of the dorsomedial visual area: pathways for early integration of dorsal and ventral streams in extrastriate cortex. J Neurosci 29:4548-4563.
83. Rouiller EM, Tanne J, Moret V, Boussaoud D. 1999. Origin of thalamic inputs to the primary, premotor, and supplementary motor cortical areas and to area 46 in macaque monkeys: a multiple retrograde tracing study. J Comp Neurol 409:131-152.
84. Rozzi S, Calzavara R, Belmalih A, Borra E, Gregoriou GG, Matelli M, Luppino G. 2006. Cortical connections of the inferior parietal cortical convexity of the macaque monkey. Cereb Cortex 16:1389-1417.
85. Rozzi S, Ferrari PF, Bonini L, Rizzolatti G, Fogassi L. 2008. Functional organization of inferior parietal lobule convexity in the macaque monkey: electrophysiological characterization of motor, sensory and mirror responses and their correlation with cytoarchitectonic areas. Eur J Neurosci 28:1569-1588.
86. Schmued L, Kyriakidis K, Heimer L. 1990. In vivo anterograde and retrograde axonal transport of the fluorescent rhodaminedextranamine, Fluoro-Ruby, within the CNS. Brain Res 526:127-134.
87. Sereno MI, Huang RS. 2014. Multisensory maps in parietal cortex. Curr Opin Neurobiol 24:39-46.
88. Siegel S. 1956. Nonparametric statistics for the behavioral sciences. New York: McGraw-Hill.
89. Stanton GB, Freidman HR, Dias EC, Bruce CJ. 2005. Cortical afferents to the smooth-pursuit region of the macaque monkey's frontal eyefield. Exp Brain Res 165:179-192.
90. Stepniewska I, Preuss TM, Kaas JH. 1994. Architectonic subdivisions of the motor thalamus of owl monkeys: Nissl, acetylcholinesterase, and cytochrome oxidase patterns. J Comp Neurol 349:536-357.
91. Stepniewska I, Preuss TM, Kaas JH. 2006. Ipsilateral cortical connections of dorsal and ventral premotor areas in new world owl monkeys. J Comp Neurol 495:691-708.
92. Stepniewska I, Preuss TM, Kaas JH. 2007. Thalamic connections of the dorsal and ventral premotor areas in New World owl monkeys. Neuroscience 147:727-745.
93. Striedter GF. 2005. Principles of brain evolution. Sunderland, MA: Sinauer.
94. Tanaka M, Fukushima K. 1998. Neuronal responses related to smooth pursuit eye movements in the periarcuate cortical area of monkeys. J Neurophysiol 80:28-47.
95. Tanné-Gariépy J, Rouiller EM, Boussaoud D. 2002. Parietal inputs to dorsal versus ventral premotor areas in the macaque monkey: evidence for largely segregated visuomotor pathways. Exp Brain Res 145:91-103.
96. 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.
97. Virley D, Hadingham SJ, Roberts JC, Farnfield B, Elliott H, Whelan G, Golder J, David C, Parsons AA, Hunter AJ. 2004. A new primate model of focal stroke: endothelin-1-induced middle cerebral artery occlusion and reperfusion in the common marmoset. J Cereb Blood Flow Metab 24:24-41.
98. Vogt C, Vogt O. 1919. Allegmeinere Ergebnisse unserer Hirnforschung. J Psychol Neurol (Leipzig) 25:279-439.
99. Wang Y, Shima K, Isoda M, Sawamura H, Tanji J. 2002. Spatial distribution and density of prefrontal cortical cells projecting to three sectors of the premotor cortex. Neuroreport 13:1341-1344.
100. Wong-Riley M. 1979. Changes in the visual system of monocularly sutured or enucleated cats demonstrable with cytochrome oxidase histochemistry. Brain Res 171:11-28.
101. Wu CW, Bichot NP, Kaas JH. 2000. Converging evidence from microstimulation, architecture, and connections for multiple motor areas in the frontal and cingulate cortex of prosimian primates. J Comp Neurol 423:140-177.
102. Yamane J, Nakamura M, Iwanami A, Sakaguchi M, Katoh H, Yamada M, Momoshima S, Miyao S, Ishii K, Tamaoki N, Nomura T, Okano HJ, Kanemura Y, Toyama Y, Okano H. 2010. Transplantation of galectin-1-expressing human neural stem cells into the injured spinal cord of adult common marmosets. J Neurosci Res 88:1394-405.
103. Yokochi H, Tanaka M, Kumashiro M, Iriki A. 2003. Inferior parietal somatosensory neurons coding face-hand coordination in Japanese macaques. Somatosens Mot Res 20:115-125.