Brain Structure and Function

, Volume 223, Issue 4, pp 1713–1729 | Cite as

Cortical and subcortical connections of parietal and premotor nodes of the monkey hand mirror neuron network

  • Stefania Bruni
  • Marzio Gerbella
  • Luca Bonini
  • Elena Borra
  • Gino Coudé
  • Pier Francesco Ferrari
  • Leonardo Fogassi
  • Monica Maranesi
  • Francesca Rodà
  • Luciano Simone
  • Francesca Ugolotti Serventi
  • Stefano Rozzi
Original Article

Abstract

Mirror neurons (MNs) are a class of cells originally discovered in the monkey ventral premotor cortex (PMv) and inferior parietal lobule (IPL). They discharge during both action execution and action observation and appear to play a crucial role in understanding others’ actions. It has been proposed that the mirror mechanism is based on a match between the visual description of actions, encoded in temporal cortical regions, and their motor representation, provided by PMv and IPL. However, neurons responding to action observation have been recently found in other cortical regions, suggesting that the mirror mechanism relies on a wider network. Here we provide the first description of this network by injecting neural tracers into physiologically identified IPL and PMv sectors containing hand MNs. Our results show that these sectors are reciprocally connected, in line with the current view, but IPL MN sectors showed virtually no direct connection with temporal visual areas. In addition, we found that PMv and IPL MN sectors share connections with several cortical regions, including the dorsal and mesial premotor cortex, the primary motor cortex, the secondary somatosensory cortex, the mid-dorsal insula and the ventrolateral prefrontal cortex, as well as subcortical structures, such as motor and polysensory thalamic nuclei and the mid-dorsal claustrum. We propose that each of these regions constitutes a node of an “extended network”, through which information relative to ongoing movements, social context, environmental contingencies, abstract rules, and internal states can influence MN activity and contribute to several socio-cognitive functions.

Keywords

Grasping Action observation Action recognition Anatomical connections Motor Parietal 

Notes

Acknowledgements

The research was supported by the European Commission Grant Cogsystems (FP7- 250013), Italian PRIN (prot. 2010MEFNF7), Interuniversity Attraction Poles (IAP) P7/11, and Istituto Italiano di Tecnologia (IIT). We thank G. Luppino for early discussion of the data and his valuable comments on an early version of the manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare no competing financial interests.

References

  1. Alegre M, Rodríguez-Oroz MC, Valencia M et al (2010) Changes in subthalamic activity during movement observation in Parkinson’s disease: is the mirror system mirrored in the basal ganglia? Clin Neurophysiol 121:414–425.  https://doi.org/10.1016/j.clinph.2009.11.013 CrossRefPubMedGoogle Scholar
  2. Arbib MA, Mundhenk TN (2005) Schizophrenia and the mirror system: an essay. Neuropsychologia 43(2):268–80.  https://doi.org/10.1016/j.neuropsychologia.2004.11.013
  3. Barraclough NE, Keith RH, Xiao D et al (2009) Visual adaptation to goal-directed hand actions. J Cogn Neurosci 21:1805–1819.  https://doi.org/10.1162/jocn.2008.21145 CrossRefGoogle Scholar
  4. Belmalih A, Borra E, Contini M et al (2009) Multimodal architectonic subdivision of the rostral part (area F5) of the macaque ventral premotor cortex. J Comp Neurol 512:183–217.  https://doi.org/10.1002/cne.21892 CrossRefPubMedGoogle Scholar
  5. Bettio F, Demelio S, Gobbetti E et al (2001) Interactive 3-D reconstruction and visualization of primates cerebral cortex. Soc Neurosci Abstr, Program No. 728.724Google Scholar
  6. Bonini L (2016) The extended mirror neuron network: anatomy, origin, and functions. Neurosci 23:56–67.  https://doi.org/10.1177/1073858415626400 (Review) Google Scholar
  7. Bonini L, Rozzi S, Serventi FU et al (2010) Ventral premotor and inferior parietal cortices make distinct contribution to action organization and intention understanding. Cereb Cortex 20:1372–1385.  https://doi.org/10.1093/cercor/bhp200 CrossRefPubMedGoogle Scholar
  8. Borra E, Belmalih A, Calzavara R et al (2008) Cortical connections of the macaque anterior intraparietal (AIP) area. Cereb Cortex 18:1094–1111.  https://doi.org/10.1093/cercor/bhm146 CrossRefPubMedGoogle Scholar
  9. Borra E, Gerbella M, Rozzi S, Luppino G (2011) Anatomical evidence for the involvement of the macaque ventrolateral prefrontal area 12r in controlling goal-directed actions. J Neurosci.  https://doi.org/10.1523/JNEUROSCI.1745-11.2011 PubMedCentralGoogle Scholar
  10. Borra E, Gerbella M, Rozzi S, Luppino G (2017) The macaque lateral grasping network: a neural substrate for generating purposeful hand actions. Neurosci Biobehav Rev 75:65–90.  https://doi.org/10.1016/j.neubiorev.2017.01.017 CrossRefPubMedGoogle Scholar
  11. Bruni S, Giorgetti V, Bonini L, Fogassi L (2015) Processing and Integration of Contextual Information in Monkey Ventrolateral Prefrontal Neurons during Selection and Execution of Goal-Directed Manipulative Actions. J Neurosci 35:11877–11890.  https://doi.org/10.1523/JNEUROSCI.1938-15.2015 CrossRefPubMedGoogle Scholar
  12. Buys EJ, Lemon RN, Mantel GWH, Muirt RB (1986) Selective facilitation of different hand muscles by single corticospinal neurones in the conscious monkey. J Physiol 381:529–549.  https://doi.org/10.1113/jphysiol.1986.sp016342 CrossRefPubMedPubMedCentralGoogle Scholar
  13. Caligiore D, Pezzulo G, Miall RC, Baldassarre G (2013) The contribution of brain sub-cortical loops in the expression and acquisition of action understanding abilities. Neurosci Biobehav Rev 37:2504–2515.  https://doi.org/10.1016/j.neubiorev.2013.07.016 CrossRefPubMedPubMedCentralGoogle Scholar
  14. Cappe C, Morel A, Barone P, Rouiller EM (2009) The thalamocortical projection systems in primate: an anatomical support for multisensory and sensorimotor interplay. Cereb Cortex Sept 19:2025–2037.  https://doi.org/10.1093/cercor/bhn228 CrossRefGoogle Scholar
  15. Carmichael ST, Price JL (1994) Architectonic subdivision of the orbital and medial prefrontal cortex in the macaque monkey. J Comp Neurol 346:366–402.  https://doi.org/10.1002/cne.903460305 CrossRefPubMedGoogle Scholar
  16. Chalfin BP, Cheung DT, Muniz JA, de Lima Silveira LC, Finlay BL (2007) Scaling of neuron number and volume of the pulvinar complex in New World primates: comparisons with humans, other primates, and mammals. J Comp Neurol 504(3):265–274.  https://doi.org/10.1002/cne.21406 CrossRefPubMedGoogle Scholar
  17. Cisek P, Kalaska JF (2004) Neural correlates of mental rehearsal in dorsal premotor cortex. Nature 431:993–996.  https://doi.org/10.1038/nature03005 CrossRefPubMedGoogle Scholar
  18. Contini M, Baccarini M, Borra E et al (2010) Thalamic projections to the macaque caudal ventrolateral prefrontal areas 45A and 45B. Eur J Neurosci 32:1337–1353.  https://doi.org/10.1111/j.1460-9568.2010.07390.x CrossRefPubMedGoogle Scholar
  19. de Gelder B, Huis In ‘t Veld EM, Van den Stock J (2015) The Facial expressive action stimulus test. A test battery for the assessment of face memory, face and object perception, configuration processing, and facial expression recognition. Front Psychol 6:1609.  https://doi.org/10.3389/fpsyg.2015.01609 CrossRefPubMedPubMedCentralGoogle Scholar
  20. di Pellegrino U, Fadiga L, Fogassi L et al (1992) Experimental brain research 9. Exp Brain Res 176–180.  https://doi.org/10.1007/bf00230027
  21. Di Cesare G, Di Dio C, Marchi M et al (2015) Expressing our internal states and understanding those of others. Proc Natl Acad Sci USA 112(33):10331–10335.  https://doi.org/10.1073/pnas.1512133112 CrossRefPubMedPubMedCentralGoogle Scholar
  22. Dum RP, Strick PL (2003) An unfolded map of the cerebellar dentate nucleus and its projections to the cerebral cortex. J Neurophysiol 89(1):634–639.  https://doi.org/10.1152/jn.00626.2002 CrossRefPubMedGoogle Scholar
  23. Dushanova J, Donoghue J (2010) Neurons in primary motor cortex engaged during action observation. Eur J Neurosci 31(2):386–398.  https://doi.org/10.1111/j.1460-9568.2009.07067.x CrossRefPubMedPubMedCentralGoogle Scholar
  24. Evangeliou MN, Raos V, Galletti C, Savaki HE (2009) Functional imaging of the parietal cortex during action execution and observation. Cereb Cortex 19:624–639.  https://doi.org/10.1093/cercor/bhn116 CrossRefPubMedGoogle Scholar
  25. Fagg AH, Arbib MA (1998) Modeling parietal–premotor interactions in primate control of grasping. Neural Networks 11:1277–1303.  https://doi.org/10.1016/S0893-6080(98)00047-1 CrossRefPubMedGoogle Scholar
  26. Ferrari PF, Bonini L, Fogassi L (2009) From monkey mirror neurons to primate behaviours: possible “direct” and “indirect” pathways. Philos Trans R Soc Lond B Biol Sci 364(1528):2311–2323.  https://doi.org/10.1098/rstb.2009.0062 CrossRefPubMedPubMedCentralGoogle Scholar
  27. Ferrari PF, Gerbella M, Coudé G, Rozzi S. (2017) Two different mirror neuron networks: the sensorimotor (hand) and limbic (face) pathways. Neuroscience 358(49):300–315.  10.1016/j.neuroscience.2017.06.052 CrossRefPubMedGoogle Scholar
  28. Fitzgerald PJ, Lane JW, Thakur PH, Hsiao SS (2004) Receptive field properties of the macaque second somatosensory cortex: evidence for multiple functional representations. J Neurosci 24(49):11193–11204.  https://doi.org/10.1523/JNEUROSCI.3481-04.2004 CrossRefPubMedPubMedCentralGoogle Scholar
  29. Fogassi L, Ferrari PF, Gesierich B et al (2005) Parietal Lobe: From Action Organization to Intention Understanding. Science 308(5722):662–667.  https://doi.org/10.1126/science.1106138 CrossRefPubMedGoogle Scholar
  30. Frey S, Mackey S (2014) Cortico-cortical connections of areas 44 and 45B in the macaque monkey. Brain Lang 131:36–55.  https://doi.org/10.1016/j.bandl.2013.05.005 CrossRefPubMedGoogle Scholar
  31. Gallese V, Fadiga L, Fogassi L, Rizzolatti G (1996) Action recognition in the premotor cortex. Brain Lang 119:593–609CrossRefGoogle Scholar
  32. Gattass R, Soares JGM, Desimone R et al (2014) Connectional subdivision of the claustrum: two visuotopic subdivisions in the macaque. Front Syst Neurosci 8:63.  https://doi.org/10.3389/fnsys.2014.00063 CrossRefPubMedPubMedCentralGoogle Scholar
  33. Gazzola V, Keysers C (2009) The Observation and execution of actions share motor and somatosensory voxels in all tested subjects: single-subject analyses of unsmoothed fMRI data. Cereb Cortex June 19:1239–1255.  https://doi.org/10.1093/cercor/bhn181 CrossRefGoogle Scholar
  34. Gerbella M, Belmalih A, Borra E et al (2007) Multimodal architectonic subdivision of the caudal ventrolateral prefrontal cortex of the macaque monkey. Brain Struct Funct 212:269–301.  https://doi.org/10.1007/s00429-007-0158-9 CrossRefPubMedGoogle Scholar
  35. Gerbella M, Belmalih A, Borra E et al (2011) Cortical connections of the anterior (F5a) subdivision of the macaque ventral premotor area F5. Brain Struct Funct 216:43–65.  https://doi.org/10.1007/s00429-010-0293-6 CrossRefPubMedGoogle Scholar
  36. Gerbella M, Borra E, Tonelli S et al (2013) Connectional heterogeneity of the ventral part of the macaque area 46. Cereb Cortex 23:967–987.  https://doi.org/10.1093/cercor/bhs096 CrossRefPubMedGoogle Scholar
  37. Gerbella M, Baccarini M, Borra E et al (2014) Amygdalar connections of the macaque areas 45A and 45B. Brain Struct Funct 219:831–842.  https://doi.org/10.1007/s00429-013-0538-2 CrossRefPubMedGoogle Scholar
  38. Gerbella M, Borra E, Mangiaracina C et al (2016a) Corticostriate projections from areas of the “lateral grasping network”: evidence for multiple hand-related input channels. Cereb Cortex 26:3096–3115.  https://doi.org/10.1093/cercor/bhv135 CrossRefPubMedGoogle Scholar
  39. Gerbella M, Borra E, Rozzi S, Luppino G (2016b) Connections of the macaque granular frontal opercular (GrFO) area: a possible neural substrate for the contribution of limbic inputs for controlling hand and face/mouth actions. Brain Struct Funct 221:59–78.  https://doi.org/10.1007/s00429-014-0892-8 CrossRefPubMedGoogle Scholar
  40. Gharbawie OA, Stepniewska I, Kaas JH (2011) Cortical connections of functional zones in posterior parietal cortex and frontal cortex motor regions in new world monkeys. Cereb Cortex 21:1981–2002.  https://doi.org/10.1093/cercor/bhq260 CrossRefPubMedPubMedCentralGoogle Scholar
  41. 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.  https://doi.org/10.1002/CNE.20933 CrossRefPubMedGoogle Scholar
  42. Haroush K, Williams ZM (2015) Neuronal prediction of opponent’s behavior during cooperative social interchange in primates. Cell 160:1–13.  https://doi.org/10.1016/j.cell.2015.01.045 CrossRefGoogle Scholar
  43. Hihara S, Taoka M, Tanaka M, Iriki A (2015) Visual responsiveness of neurons in the secondary somatosensory area and its surrounding parietal operculum regions in awake macaque monkeys. Cereb Cortex.  https://doi.org/10.1093/cercor/bhv095 PubMedPubMedCentralGoogle Scholar
  44. Hoshi E, Shima K, Tanji J (1998) Task-dependent selectivity of movement-related neuronal activity in the primate prefrontal cortex. J Neurophysiol 80(6):3392–3397. https://jn.physiology.org/content/80/6/3392.long CrossRefPubMedGoogle Scholar
  45. Ishida H, Suzuki K, Grandi LC (2015) Predictive coding accounts of shared representations in parieto-insular networks. Neuropsychologia 70:442–454.  https://doi.org/10.1016/j.neuropsychologia.2014.10.020 CrossRefPubMedGoogle Scholar
  46. Jellema T, Perrett DI (2006) Neural representations of perceived bodily actions using a categorical frame of reference. Neuropsychologia 44:1535–1546.  https://doi.org/10.1016/j.neuropsychologia.2006.01.020 CrossRefPubMedGoogle Scholar
  47. Jezzini A, Caruana F, Stoianov I et al (2012) Functional organization of the insula and inner perisylvian regions. Proc Natl Acad Sci U S A 109(25):10077–10082.  https://doi.org/10.1073/pnas.1200143109 CrossRefPubMedPubMedCentralGoogle Scholar
  48. Jezzini A, Rozzi S, Borra E et al (2015) A shared neural network for emotional expression and perception: an anatomical study in the macaque monkey. Front Behav Neurosci 9:243.  https://doi.org/10.3389/fnbeh.2015.00243 CrossRefPubMedPubMedCentralGoogle Scholar
  49. Kaas JH, Lyon DC (2007) Pulvinar contributions to the dorsal and ventral streams of visual processing in primates. Brain Res Rev 55(2):285–296.  https://doi.org/10.1016/j.brainresrev.2007.02.008 CrossRefPubMedPubMedCentralGoogle Scholar
  50. Kraskov A, Dancause N, Quallo MM et al (2009) Corticospinal neurons in macaque ventral premotor cortex with mirror properties: a potential mechanism for action suppression? Neuron 64:922–930.  https://doi.org/10.1016/j.neuron.2009.12.010 CrossRefPubMedPubMedCentralGoogle Scholar
  51. Kraskov A, Prabhu G, Quallo M et al (2011) Ventral premotor-motor cortex interactions in the macaque monkey during grasp: response of single neurons to intracortical microstimulation. J Neurosci 31(24):8812–8821.  https://doi.org/10.1523/JNEUROSCI.0525-11.2011 CrossRefPubMedPubMedCentralGoogle Scholar
  52. 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 428:112–137CrossRefPubMedGoogle Scholar
  53. Luppino G, Matelli M, Camarda RM et al (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.  https://doi.org/10.1002/cne.903110403 CrossRefPubMedGoogle Scholar
  54. 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 F5 and F4). Exp brain Res 128:181–187.  https://doi.org/10.1007/s002210050833 CrossRefPubMedGoogle Scholar
  55. Luppino G, Rozzi S, Calzavara R, Matelli M (2003) Prefrontal and agranular cingulate projections to the dorsal premotor areas F2 and F7 in the macaque monkey. Eur J Neurosci 17:559–578.  https://doi.org/10.1046/j.1460-9568.2003.02476.x CrossRefPubMedGoogle Scholar
  56. Luppino G, Hamed SB, Gamberini M et al (2005) Occipital (V6) and parietal (V6A) areas in the anterior wall of the parieto-occipital sulcus of the macaque: a cytoarchitectonic study. Eur J Neurosci 21:3056–3076.  https://doi.org/10.1111/j.1460-9568.2005.04149.x CrossRefPubMedGoogle Scholar
  57. Maeda K, Ishida H, Nakajima K et al (2015) Functional properties of parietal hand manipulation-related neurons and mirror neurons responding to vision of own hand action. J Cogn Neurosci 27:560–572.  https://doi.org/10.1162/jocn_a_00742 CrossRefPubMedGoogle Scholar
  58. Maier MA, Kirkwood PA, Brochier T, Lemon RN (2013) Responses of single corticospinal neurons to intracortical stimulation of primary motor and premotor cortex in the anesthetized macaque monkey. J Neurophysiol 109(12):2982–2998.  https://doi.org/10.1152/jn.01080.2012 CrossRefPubMedPubMedCentralGoogle Scholar
  59. Maranesi M, Rodà F, Bonini L et al (2012) Anatomo-functional organization of the ventral primary motor and premotor cortex in the macaque monkey. Eur J Neurosci 36:3376–3387.  https://doi.org/10.1111/j.1460-9568.2012.08252.x CrossRefPubMedGoogle Scholar
  60. Maranesi M, Ugolotti Serventi F, Bruni S et al (2013) Monkey gaze behaviour during action observation and its relationship to mirror neuron activity. Eur J Neurosci 38:3721–3730.  https://doi.org/10.1111/ejn.12376 CrossRefPubMedGoogle Scholar
  61. Matelli M, Luppino G (1996) Thalamic input to mesial and superior area 6 in the macaque monkey. J Comp Neurol 372:59–87CrossRefPubMedGoogle Scholar
  62. 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.  https://doi.org/10.1016/0166-4328(85)90068-3 CrossRefPubMedGoogle Scholar
  63. 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.  https://doi.org/10.1002/cne.902510302 CrossRefPubMedGoogle Scholar
  64. Matelli M, Luppino G, Fogassi L, Rizzolatti G (1989) Thalamic input to inferior area 6 and area 4 in the macaque monkey. J Comp Neurol 280:468–488.  https://doi.org/10.1002/cne.902800311 CrossRefPubMedGoogle Scholar
  65. 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.  https://doi.org/10.1002/cne.903110402 CrossRefPubMedGoogle Scholar
  66. Matelli M, Govoni P, Galletti C et al (1998) Superior area 6 afferents from the superior parietal lobule in the macaque monkey. J Comp Neurol 402:327–352CrossRefPubMedGoogle Scholar
  67. Nelissen K, Luppino G, Vanduffel W et al (2005) Observing others: multiple action representation in the frontal lobe. Science 310(5746):332–336.  https://doi.org/10.1126/science.1115593 CrossRefPubMedGoogle Scholar
  68. Nelissen K, Borra E, Gerbella M et al (2011) Action observation circuits in the macaque monkey cortex. J Neurosci 31(10):3743–3756.  https://doi.org/10.1523/JNEUROSCI.4803-10.2011 CrossRefPubMedPubMedCentralGoogle Scholar
  69. Ohbayashi M, Picard N, Strick PL (2016) Inactivation of the dorsal premotor area disrupts internally generated, but not visually guided, sequential movements. J Neurosci 36(6):1971–1976.  https://doi.org/10.1523/JNEUROSCI.2356-15.2016 CrossRefPubMedPubMedCentralGoogle Scholar
  70. Olszewski J (1952) The thalamus of Macaca Mulatta. S. Karger, New YorkGoogle Scholar
  71. Pandya DN, Seltzer B (1982) Intrinsic connections and architectonics of posterior parietal cortex in the rhesus monkey. J Comp Neurol 204:196–210.  https://doi.org/10.1002/cne.902040208 CrossRefPubMedGoogle Scholar
  72. Pani P, Theys T, Romero MC, Janssen P (2014) Grasping execution and grasping observation activity of single neurons in the macaque anterior intraparietal area. J Cogn Neurosci 26:2342–2355.  https://doi.org/10.1162/jocn_a_00647 CrossRefPubMedGoogle Scholar
  73. Perrett DI, Harries MH, Bevan R et al (1989) Frameworks of analysis for the neural representation of animate objects and actions. J Exp Biol 146:87–113PubMedGoogle Scholar
  74. 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.  https://doi.org/10.1002/cne.902280110 CrossRefPubMedGoogle Scholar
  75. Raos V, Savaki HE (2016) Perception of actions performed by external agents presupposes knowledge about the relationship between action and effect. Neuroimage 132:261–273.  https://doi.org/10.1016/j.neuroimage.2016.02.023 CrossRefPubMedGoogle Scholar
  76. 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(3):1503–1518.  https://doi.org/10.1152/jn.00661.2002 CrossRefPubMedGoogle Scholar
  77. Rathelot J-A, Strick PL (2009) Subdivisions of primary motor cortex based on cortico-motoneuronal cells. Proc Natl Acad Sci U S A 106:918–923.  https://doi.org/10.1073/pnas.0808362106 CrossRefPubMedPubMedCentralGoogle Scholar
  78. Ray JP, Price JL (1993) The organization of projections from the mediodorsal nucleus of the thalamus to orbital and medial prefrontal cortex in macaque monkeys. J Comp Neurol 337:1–31.  https://doi.org/10.1002/cne.903370102 CrossRefPubMedGoogle Scholar
  79. Rizzolatti G, Fogassi L (2014) The mirror mechanism: recent findings and perspectives. Philos Trans R Soc Lond B Biol Sci 369(1644):20130420.  https://doi.org/10.1098/rstb.2013.0420 CrossRefPubMedPubMedCentralGoogle Scholar
  80. Rizzolatti G, Wolpert DM (2005) Motor systems. Curr Opin Neurobiol 15:623–625.  https://doi.org/10.1016/j.conb.2005.10.018 CrossRefPubMedGoogle Scholar
  81. Rizzolatti G, Fadiga L, Gallese V, Fogassi L (1996) Premotor cortex and the recognition of motor actions. Brain Res Cogn Brain Res 3:131–141.  https://doi.org/10.1016/0926-6410(95)00038-0 CrossRefPubMedGoogle Scholar
  82. Robinson CJ, Burton H (1980) Somatotopographic organization in the second somatosensory area ofM. fascicularis. J Comp Neurol 192:43–67.  https://doi.org/10.1002/cne.901920104 CrossRefPubMedGoogle Scholar
  83. Rozzi S, Fogassi L (2017) Neural coding for action execution and action observation in the prefrontal cortex and its role in the organization of socially driven behavior. Front Neurosci 11:492.  https://doi.org/10.3389/fnins.2017.00492 CrossRefPubMedPubMedCentralGoogle Scholar
  84. Rozzi S, Calzavara R, Belmalih A et al (2006) Cortical connections of the inferior parietal cortical convexity of the macaque monkey. Cereb Cortex 16(10):1389–1417.  https://doi.org/10.1093/cercor/bhj076 CrossRefPubMedGoogle Scholar
  85. Rozzi S, Ferrari PF, Bonini L et al (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.  https://doi.org/10.1111/j.1460-9568.2008.06395.x CrossRefPubMedGoogle Scholar
  86. Russchen FT, Amaral DG, Price JL (1987) The afferent input to the magnocellular division of the mediodorsal thalamic nucleus in the monkey, Macaca fascicularis. J Comp Neurol 256:175–210.  https://doi.org/10.1002/cne.902560202 CrossRefPubMedGoogle Scholar
  87. Schieber M, Hibbard L (1993) How somatotopic is the motor cortex hand area? Science 261(5120):489–492CrossRefPubMedGoogle Scholar
  88. Schieber MH, Santello M (2004) Hand function: peripheral and central constraints on performance. J Appl Physiol (1985) 96(6):2293–2300.  https://doi.org/10.1152/japplphysiol.01063.2003 CrossRefPubMedGoogle Scholar
  89. 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.  https://doi.org/10.1016/0006-8993(78)90584-X CrossRefPubMedGoogle Scholar
  90. Seltzer B, Pandya DN (1984) Further observations on parieto-temporal connections in the rhesus monkey. Exp brain Res 55:301–312.  https://doi.org/10.1007/BF00237280 CrossRefPubMedGoogle Scholar
  91. Sherman SM (2007) The thalamus is more than just a relay. Curr Opin Neurobiol 17(4):417–422.  https://doi.org/10.1016/j.conb.2007.07.003 CrossRefPubMedPubMedCentralGoogle Scholar
  92. Simone L, Rozzi S, Bimbi M, Fogassi L (2015) Movement-related activity during goal-directed hand actions in the monkey ventrolateral prefrontal cortex. Eur J Neurosci 42:2882–2894.  https://doi.org/10.1111/ejn.13040 CrossRefPubMedGoogle Scholar
  93. Simone L, Bimbi M, Rodà F et al (2017) Action observation activates neurons of the monkey ventrolateral prefrontal cortex. Sci Rep 14 7:44378.  https://doi.org/10.1038/srep44378 (Nat Publ Gr) CrossRefPubMedPubMedCentralGoogle Scholar
  94. Tanji J, Hoshi E (2008) Role of the lateral prefrontal cortex in executive behavioral control. Physiol Rev 88(1):37–57.  https://doi.org/10.1152/physrev.00014.2007 CrossRefPubMedGoogle Scholar
  95. Tanné-Gariépy J, Boussaoud D, Rouiller EM (2002) Projections of the claustrum to the primary motor, premotor, and prefrontal cortices in the macaque monkey. J Comp Neurol 454:140–157.  https://doi.org/10.1002/cne.10425 CrossRefPubMedGoogle Scholar
  96. Tkach D, Reimer J, Hatsopoulos NG (2007) Congruent Activity during Action and Action Observation in Motor Cortex. J Neurosci 27(48):13241–13250.  https://doi.org/10.1523/JNEUROSCI.2895-07.2007 CrossRefPubMedGoogle Scholar
  97. Ubaldi S, Barchiesi G, Cattaneo L (2015) Bottom-up and top-down visuomotor responses to action observation. Cereb Cortex 25:1032–1041.  https://doi.org/10.1093/cercor/bht295 CrossRefPubMedGoogle Scholar
  98. Vigneswaran G, Philipp R, Lemon RN, Kraskov A (2013) M1 corticospinal mirror neurons and their role in movement suppression during action observation. Curr Biol.  https://doi.org/10.1016/j.cub.2012.12.006 PubMedPubMedCentralGoogle Scholar
  99. Walker E (1940) A cytoarchitectural study of the prefrontal area of the macaque monkey. J Comp Neurol 98:59–86. doi:  https://doi.org/10.1002/cne.900730106 CrossRefGoogle Scholar
  100. Wolpert DM, Miall RC, Kawato M (1998) Internal models in the cerebellum. Trends Cogn Sci.  https://doi.org/10.1016/S1364-6613(98)01221-2 PubMedGoogle Scholar
  101. Yoshida K, Saito N, Iriki A, Isoda M (2011) Report Representation of Others’ Action by Neurons in Monkey Medial Frontal Cortex. Curr Biol 21:249–253. doi:  https://doi.org/10.1016/j.cub.2011.01.004 CrossRefPubMedGoogle Scholar
  102. Yoshida K, Saito N, Iriki A, Isoda M (2012) Social error monitoring in macaque frontal cortex. Nat Neurosci 15:1307–1312. doi:  https://doi.org/10.1038/nn.3180 CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2017

Authors and Affiliations

  • Stefania Bruni
    • 1
    • 2
  • Marzio Gerbella
    • 1
    • 3
  • Luca Bonini
    • 1
  • Elena Borra
    • 1
  • Gino Coudé
    • 4
  • Pier Francesco Ferrari
    • 1
    • 4
  • Leonardo Fogassi
    • 1
  • Monica Maranesi
    • 1
  • Francesca Rodà
    • 1
  • Luciano Simone
    • 5
  • Francesca Ugolotti Serventi
    • 1
  • Stefano Rozzi
    • 1
  1. 1.Department of Medicine and Surgery, Unit of NeuroscienceUniversity of ParmaParmaItaly
  2. 2.Department of NeuroscienceBaylor College of MedicineHoustonUSA
  3. 3.Center for Biomolecular NanotechnologiesIstituto Italiano di TecnologiaLecceItaly
  4. 4.Institut des Sciences Cognitives Marc Jeannerod UMR 5229, CNRSUniversité Claude Bernard Lyon 1Bron CedexFrance
  5. 5.Center for Translational NeurophysiologyIstituto Italiano di TecnologiaFerraraItaly

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