Experimental Brain Research

, Volume 237, Issue 12, pp 3375–3390 | Cite as

The role of cortical areas hMT/V5+ and TPJ on the magnitude of representational momentum and representational gravity: a transcranial magnetic stimulation study

  • Nuno Alexandre De Sá TeixeiraEmail author
  • Gianfranco Bosco
  • Sergio Delle Monache
  • Francesco Lacquaniti
Research Article


The perceived vanishing location of a moving target is systematically displaced forward, in the direction of motion—representational momentum—, and downward, in the direction of gravity—representational gravity. Despite a wealth of research on the factors that modulate these phenomena, little is known regarding their neurophysiological substrates. The present experiment aims to explore which role is played by cortical areas hMT/V5+, linked to the processing of visual motion, and TPJ, thought to support the functioning of an internal model of gravity, in modulating both effects. Participants were required to perform a standard spatial localization task while the activity of the right hMT/V5+ or TPJ sites was selectively disrupted with an offline continuous theta-burst stimulation (cTBS) protocol, interspersed with control blocks with no stimulation. Eye movements were recorded during all spatial localizations. Results revealed an increase in representational gravity contingent on the disruption of the activity of hMT/V5+ and, conversely, some evidence suggested a bigger representational momentum when TPJ was stimulated. Furthermore, stimulation of hMT/V5+ led to a decreased ocular overshoot and to a time-dependent downward drift of gaze location. These outcomes suggest that a reciprocal balance between perceived kinematics and anticipated dynamics might modulate these spatial localization responses, compatible with a push–pull mechanism.


Representational momentum Representational gravity Medio-temporal area Temporo-parietal junction Theta-burst stimulation 



This work was supported by the Italian Space Agency (grants I/006/06/0 and MARS-PRE) and the Italian University Ministry (PRIN grants 2015HFWRYY_002, 2017KZNZLN_003 and 2017CBF8NJ_005).


  1. Amorim MA, Lang W, Lindinger G, Mayer D, Deecke L, Berthoz A (2000) Modulation of spatial orientation by mental imagery: a MEG study of representational momentum. J Cogni Neurosci 12:569–582Google Scholar
  2. Ashida H (2004) Action-specific extrapolation of target motion in human visual system. Neuropsychologia 42:1515–1524PubMedGoogle Scholar
  3. Barton JJ, Sharpe JA, Raymond JE (1996) Directional defects in pursuit and motion perception in humans with unilateral cerebral lesions. Brain 119:1535–1550PubMedGoogle Scholar
  4. Bertamini M (1993) Memory for position and dynamic representations. Mem Cognit 21:449–457PubMedGoogle Scholar
  5. Born RT, Bradley DC (2005) Structure and function of visual area MT. Ann Rev Neurosci 28:157–189PubMedGoogle Scholar
  6. Bosco G, Carrozzo M, Lacquaniti F (2008) Contributions of the human temporo-parietal junction and MT/V5 + to the timing of interception revealed by TMS. J Neurosci 28:12071–12084PubMedPubMedCentralGoogle Scholar
  7. Bosco G, Delle Monache S, Lacquaniti F (2012) Catching what we cannot see: manual interception of occluded fly-ball trajectories. PLoS One 7:e49381PubMedPubMedCentralGoogle Scholar
  8. Bosco G, Delle Monache S, Gravano S, Indovina I, La Scaleia B, Maffei V, Zago M, Lacquaniti F (2015) Filling gaps om visual motion for target capture. Front Integr Neurosci 23:9–13Google Scholar
  9. Collewijn H, Tamminga EP (1984) Human smooth pursuit and saccadic eye movements during voluntary pursuit of different motions on different backgrounds. J Physiol (London) 351:217–250Google Scholar
  10. Corbetta N, Shulman G (2002) Control of goal-directed and stimulus-driven attention in the brain. Nat Rev Neurosci 3(3):201–215PubMedPubMedCentralGoogle Scholar
  11. Corbetta M, Patel G, Shulman G (2008) The reorienting system of the human brain: from environment to theory of mind. Neuron 58:306–354PubMedPubMedCentralGoogle Scholar
  12. De Sá Teixeira NA (2014) Fourier decomposition of spatial localization errors reveals an idiotropic dominance of an internal model of gravity. Vision Res 105:177–188PubMedGoogle Scholar
  13. De Sá Teixeira NA (2016) The visual representations of motion and of gravity are functionally independent: evidence of a differential effect of smooth pursuit eye movements. Exp Brain Res 234(9):2491–2504PubMedGoogle Scholar
  14. De Sá Teixeira NA, Hecht H (2014) Can representational trajectory reveal the nature of an internal model of gravity? Atten Percept Psychophys 76:1106–1120PubMedGoogle Scholar
  15. De Sá Teixeira NA, Hecht H, Oliveira AM (2013) The representational dynamics of remembered projectile locations. J Exp Psychol Hum Percept Perform 39:1690–1699PubMedGoogle Scholar
  16. De Sá Teixeira NA, Kerzel D, Hecht H, Lacquaniti F (2017) A novel dissociation between representational momentum and representational gravity through response modality. Psychol Res 83:1223–1236 (Epub ahead of print) PubMedGoogle Scholar
  17. Delle Monache S, Lacquaniti F, Bosco G (2014) Eye movements and manual interception of ballistic trajectories: effects of law of motion perturbations and occlusions. Exp Brain Res 233(2):359–374PubMedGoogle Scholar
  18. Delle Monache S, Lacquaniti F, Bosco G (2017) Differential contributions to the interception of occluded ballistic trajectories by the temporoparietal junction, area hMT/V5+ and the intraparietal cortex. J Neurophysiol 118(3):1809–1823PubMedPubMedCentralGoogle Scholar
  19. Fiori F, Candidi M, Acciarino A, David N, Aglioti SM (2015) The right temporoparietal junction plays a causal role in maintaining the internal representation of verticality. J Neurophysiol 114:2983–2990PubMedPubMedCentralGoogle Scholar
  20. Freyd JJ (1983) The mental representation of movement when static stimuli are viewed. Percept Psychophys 33:575–581PubMedGoogle Scholar
  21. Freyd JJ, Finke RA (1984) Representational momentum. J Exp Psychol Learn Mem Cogn 10:126–132Google Scholar
  22. Freyd JJ, Finke RA (1985) A velocity effect for representational momentum. Bull Psychono Soc 23:443–446Google Scholar
  23. Freyd JJ, Johnson JQ (1987) Probing the time course of representational momentum. J Exp Psychol Learn Mem Cogn 13:259–269PubMedGoogle Scholar
  24. Freyd JJ, Miller GF (1992) Creature motion. Bull Psychon Soc 30(6):470Google Scholar
  25. Freyd JJ, Pantzer TM (1995) Static patterns moving in the mind. In: Smith SM, Ward TB, Finke RA (eds) The creative cognition approach. MIT Press, Cambridge, pp 181–204Google Scholar
  26. Freyd JJ, Pantzer TM, Cheng JL (1988) Representing statics as forces in equilibrium. J Exp Psychol Gen 117:395–407PubMedGoogle Scholar
  27. Freyd JJ, Kelly MH, DeKay ML (1990) Representational momentum in memory for pitch. J Exp Psychol Learn Mem Cogn 16:1107–1117PubMedGoogle Scholar
  28. Getzmann S, Lewald J, Guski R (2004) Representational momentum in spatial hearing. Perception 33:591–599PubMedGoogle Scholar
  29. Hayes AE, Freyd JJ (2002) Representational momentum when attention is divided. Vis Cognit 9:8–27Google Scholar
  30. Huang ZY, Edwards MJ, Rounis E, Bhatia KP, Rothwell JC (2005) Theta burst stimulation of the human motor cortex. Neuron 45(2):201–206PubMedGoogle Scholar
  31. Hubbard TL (1990) Cognitive representation of linear motion: possible direction and gravity effects in judged displacement. Mem Cognit 18:299–309PubMedGoogle Scholar
  32. Hubbard TL (2005) Representational momentum and related displacements in spatial memory: a review of the findings. Psychon Bull Rev 12:822–851PubMedGoogle Scholar
  33. Hubbard TL (2006) Computational theory and cognition in representational momentum and related types of displacement: a reply to Kerzel. Psychon Bull Rev 13:174–177Google Scholar
  34. Hubbard TL (2010) Approaches to representational momentum: theories and models. In: Nijhawan R, Khurana B (eds) Space and time in perception and action. Cambridge University Press, Cambridge, pp 338–365Google Scholar
  35. Hubbard TL (2014) Forms of momentum across space: representational, operational, and attentional. Psychon Bull Rev 21:1371–1403PubMedGoogle Scholar
  36. Hubbard TL (2015) Forms of momentum across time: behavioral and psychological. J Mind Behav 36:47–82Google Scholar
  37. Hubbard TL, Bharucha JJ (1988) Judged displacement in apparent vertical and horizontal motion. Percept Psychophys 44:211–221PubMedGoogle Scholar
  38. Hubbard TL, Ruppel SE (2002) A possible role of naïve impetus in Michotte’s “launching effect”: evidence from representational momentum. Vis Cognit 9:153–176Google Scholar
  39. Indovina I, Maffei V, Bosco G, Zago M, Macaluso E, Lacquaniti F (2005) Representation of visual gravitational motion in the human vestibular cortex. Science 308:416–419PubMedGoogle Scholar
  40. Indovina I, Maffei V, Pauwels K, Macaluso E, Orban GA, Lacquaniti F (2013) Simulated self-motion in a visual gravity field: sensitivity to vertical and horizontal heading in the human brain. Neuroimage 71:114–124PubMedGoogle Scholar
  41. Indovina I, Mazzarella E, Maffei V, Cesqui B, Passamonti L, Lacquaniti F (2015) Sound-evoked vestibular stimulation affects the anticipation of gravity effects during visual self-motion. Exp Brain Res 233(8):2365–2371PubMedGoogle Scholar
  42. Jörges B, López-Moliner J (2017) Gravity as a strong prior: implications for perception and action. Front Hum Neurosci 11:203PubMedPubMedCentralGoogle Scholar
  43. Kelly MH, Freyd JJ (1987) Explorations of representational momentum. Cognit Psychol 19:369–401PubMedGoogle Scholar
  44. Kerzel D (2000) Eye movements and visible persistence explain the mislocalization of the final position of a moving target. Vis Res 40:3703–3715PubMedGoogle Scholar
  45. Kerzel D (2002) The locus of “memory displacement” is at least partially perceptual: effects of velocity, expectation, friction, memory averaging, and weight. Percept Psychophys 64:680–692PubMedGoogle Scholar
  46. Kerzel D (2003a) Mental extrapolation of target position is strongest with weak motion signals and motor responses. Vis Res 43:2623–2635PubMedGoogle Scholar
  47. Kerzel D (2003b) Attention maintains mental extrapolation of target position: irrelevant distractors eliminate forward displacement after implied motion. Cognition 88:109–131PubMedGoogle Scholar
  48. Kerzel D (2003c) Centripetal force draws the eyes, not memory of the target, toward the center. J Exp Psychol Learn Mem Cogn 29:458–466PubMedGoogle Scholar
  49. Kerzel D (2004) Attentional load modulates mislocalization of moving stimuli, but does not eliminate the error. Psychon Bull Rev 11(5):848–853PubMedGoogle Scholar
  50. Kerzel D (2006) Why eye movements and perceptual factors have to be controlled in studies on “Representational Momentum”. Psychol Bull Rev 13:166–173Google Scholar
  51. Kerzel D, Gegenfurtner KR (2003) Neuronal processing delays are compensated in the sensorimotor branch of the visual system. Curr Biol 13:1975–1978PubMedGoogle Scholar
  52. Kerzel D, Jordan JS, Müsseler J (2001) The role of perception in the mislocalization of the final position of a moving target. J Exp Psychol Hum Percept Perform 27:829–840PubMedGoogle Scholar
  53. Kourtzi Z, Kanwisher N (2000) Activation in human MT/MST for static images with implied motion. J Cognit Neurosci 12:48–55Google Scholar
  54. La Scaleia B, Lacquaniti F, Zago M (2014) Neural extrapolation of motion for a ball rolling down an inclined plane. PLoS One 9:e99837PubMedPubMedCentralGoogle Scholar
  55. La Scaleia B, Zago M, Lacquaniti F (2015) Hand interception of occluded motion in humans: a test of model-based vs. on-line control. J Neurophysiol 114:1577–1592PubMedPubMedCentralGoogle Scholar
  56. Lacquaniti F, Maioli C (1987) Anticipatory and reflex coactivation of antagonistic muscles in catching. Brain Res 406(1–2):373–378PubMedGoogle Scholar
  57. Lacquaniti F, Maioli C (1989) The role of preparation in tuning anticipatory and reflex responses during catching. J Neurosci 9(1):134–148PubMedPubMedCentralGoogle Scholar
  58. Lacquaniti F, Bosco G, Indovina I, La Scaleia B, Maffei V, Moscatelli A, Zago M (2013) Visual gravitational motion and the vestibular system in humans. Front Integ Neurosci 7:101Google Scholar
  59. Lacquaniti F, Bosco G, Gravano S, Indovina I, La Scaleia B, Maffei V, Zago M (2014) Multisensory integration and internal models for sensing gravity effects in primates. BioMed Res Int. CrossRefPubMedPubMedCentralGoogle Scholar
  60. Lacquaniti F, Bosco G, Gravano S, Indovina I, La Scaleia B, Maffei V, Zago M (2015) Gravity in the brain as a reference for space and time perception. Multisens Res 28:397–426PubMedGoogle Scholar
  61. Lopez C, Blanke O, Mast FW (2012) The human vestibular cortex revealed by coordinate-based activation likelihood estimation meta-analysis. Neuroscience 212:159–179PubMedGoogle Scholar
  62. Luebke AE, Robinson DA (1988) Transition dynamics between pursuit and fixation suggest different systems. Vision Res 28:941–946PubMedGoogle Scholar
  63. Maffei V, Macaluso E, Orban GA, Lacquaniti F (2010) The internal model of visual gravity contributes to interception of real and apparent motion as revealed by fMRI. J Vis 8(6):127Google Scholar
  64. Maffei V, Mazzarella E, Piras F, Spalletta G, Caltagirone C, Lacquaniti F, Daprati E (2016) Processing of visual gravitational motion in the peri-sylvian cortex: evidence from brain-damage patients. Cortex 78:55–69PubMedGoogle Scholar
  65. McGeorge P, Beschin N, Della Sala S (2006) Representing target motion: the role of the right hemispehre in the forward displacement bias. Neuropsychology 20:708–715PubMedGoogle Scholar
  66. McIntyre J, Zago M, Berthoz A, Lacquaniti F (2001) Does the brain model Newton’s laws? Nat Neurosci 4:693–694PubMedGoogle Scholar
  67. Missal M, Heinin SJ (2017) Stopping smooth pursuit. Philos Trans R Soc B 372:20160200Google Scholar
  68. Mitrani L, Dimitrov G (1978) Pursuit eye movements of a disappearing moving target. Vision Res 18:537–539PubMedGoogle Scholar
  69. Moscatelli A, Lacquaniti F (2011) The weight of time: gravitational force enhances discrimination of visual motion duration. J Vis 11(4):1–17Google Scholar
  70. Motes M, Hubbard TL, Courtney JR, Rypma B (2008) A principal components analysis of dynamic spatial memory biases. J Exp Psychol Learn Mem Cogn 34(5):1076–1083PubMedGoogle Scholar
  71. Müsseler J, Stork S, Kerzel D (2002) Comparing mislocalizations with moving stimuli: the Fröhlich effect, the flash-lag, and representational momentum. Vis Cognit 9:120–138Google Scholar
  72. Nagai M, Kazai K, Yagi A (2002) Larger forward memory displacement in the direction of gravity. Vis Cognit 9:28–40Google Scholar
  73. Orban GA, Fize D, Peuskens H, Denys K, Nelissen K, Sunaert S, Todd J, Vanduffel W (2003) Similarities and differences in motion processing between the human and macaque brain: evidence from fMRI. Neuropsychologia 41:1757–1768PubMedGoogle Scholar
  74. Pola J, Wyatt HJ (1997) Offset dynamics of human smooth pursuit eye movements: effects of target presence and subject attention. Vis Res 37(18):2579–2595PubMedGoogle Scholar
  75. Rao H, Han S, Jiang Y, Xue Y, Gu H, Cui Y, Gao D (2004) Engagement of the prefrontal cortex in representational momentum: an fMRI study. Neuroimage 23:98–103PubMedGoogle Scholar
  76. Reed CL, Vinson NG (1996) Conceptual effects on representational momentum. J Exp Psychol Hum Percept Perform 22:839–850PubMedGoogle Scholar
  77. Ridding MC, Ziemann U (2010) Determinants of the induction of cortical plasticity by non-invasive brain stimulation in healthy subjects. J Physiol 588:2291–2304PubMedPubMedCentralGoogle Scholar
  78. Riečanskỳ I (2004) Extrastriate area V5 (MT) and its role in the processing of visual motion. Ceskoslovenka Fysiologie 53(1):17–22Google Scholar
  79. Rossini PM, Burke D, Chen R, Cohen LG, Daskalakis Z, Di Iorio R, Di Lazzaro V, Ferreri F, Fitzgerald PB, George MS, Hallett M, Lefaucheur JP, Langguth B, Matsumoto H, Miniussi C, Nitsche MA, Pascual-Leone A, Paulus W, Rossi S, Rothwell JC, Siebner HR, Ugawa Y, Walsh V, Ziemann U (2015) Non-invasive electrical and magnetic stimulation of the brain, spinal cord, roots and peripheral nerves: Basis principles and procedures fro routine clinial and research application—an updated report from an I.F.C.N. Committee. Clin Neurophysiol 126(6):1071–1107PubMedPubMedCentralGoogle Scholar
  80. Rottach KG, Zivotofsky AZ, Das VE, Averbuch-Heller L, Discenna AO, Poonyathalang A, Leigh RJ (1996) Comparison of horizontal, vertical and diagonal smooth pursuit eye movements in normal human subjects. Vis Res 36:2189–2195PubMedGoogle Scholar
  81. Sacheli LM, Candidi M, Era V, Aglioti SM (2015) Causative role of left aIPS in coding shared goals during human–avatar complementary joint actions. Nat Commun 6:7544PubMedPubMedCentralGoogle Scholar
  82. Schoo LA, van Zandvoort MT, Biessels GJ, Kappelle LJ, Postma A, de Haan EH (2011) The posterior parietal paradox: why do functional magnetic resonance imaging and lesion studies on episodic memory produce conflicting results? J Neurophysiol 5:15–38Google Scholar
  83. Sekuler R, Armstrong R (1978) Fourier analysis of polar coordinate data in visual physiology and psychophysics. Behav Res Methods Instrum 10:8–14Google Scholar
  84. Senior C, Barnes J, Brammer M, Bullmore E, Giampetro V, Simmons A, David AS (1999) The functional neuroanatomy of implicit motion perception. Neuroimage 9(6):s887Google Scholar
  85. Senior C, Ward J, David AS (2002) Representational momentum and the brain: an investigation into the functional necessity of V5/MT. Vis Cognit 9:81–92Google Scholar
  86. Sestieri C, Shulman GL, Corbetta M (2010) Attention to memory and the environment: functional specialization and dynamic competition in human posterior parietal cortex. J Neurosci 30(25):8445–8456PubMedPubMedCentralGoogle Scholar
  87. Sestieri C, Shulman GL, Corbetta M (2017) The contribution of the human posterior parietal cortex to episodic memory. Nat Rev Neurosci 18(3):183–192PubMedPubMedCentralGoogle Scholar
  88. Sunaert S, Van Hecke P, Marchal G, Orban GA (1999) Motion-responsive regions of the human brain. Exp Brain Res 127(4):355–370PubMedGoogle Scholar
  89. Tanaka M, Lisberger SG (2002a) Role of arcuate frontal cortex of monkeys in smooth pursuit eye movements II: relation to vector averaging pursuit. J Neurophysiol 87:2700–2714PubMedPubMedCentralGoogle Scholar
  90. Tanaka M, Lisberger SG (2002b) Enhancement of multiple components of pursuit eye movement by microstimulation in the arcuate frontal pursuit area in monkeys. J Neurophysiol 87:802–818PubMedPubMedCentralGoogle Scholar
  91. 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(5):443–459PubMedPubMedCentralGoogle Scholar
  92. Vinson NG, Reed CL (2002) Sources of object-specific effects in representational momentum. Vis Cognit 9:41–65Google Scholar
  93. Wasserman EM (1998) Risk and safety of repetitive transcranial magnetic stimulation: report and suggested guidelines from the international workshop on the safety of repetitive transcranial magnetic stimulation, June 5-7, 1996. Electroencephalogr Clin Neurophysiol 108(1):1–16Google Scholar
  94. White H, Minor SW, Merrell J, Smith T (1993) Representational-momentum effects in the cerebral hemispheres. Brain Cognit 22:161–170Google Scholar
  95. Wischnewski M, Schutter DJLG (2015) Efficacy and time course of theta burst stimulation in healthy humans. Brain Stimul 8(4):685–692PubMedGoogle Scholar
  96. Zago M, Lacquaniti F (2005) Cognitive, perceptual and action-oriented representations of falling objects. Neuropsychologia 43(2):178–188PubMedGoogle Scholar
  97. Zeki S (2015) Area V5—a microcosm of the visual brain. Front Integ Neurosci 9:21Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Systems Medicine and Centre of Space BiomedicineUniversity of Rome ‘Tor Vergata’RomeItaly
  2. 2.Laboratory of Neuromotor PhysiologyIRCCS Santa Lucia FoundationRomeItaly
  3. 3.Department of Education and Psychology, William James Research CenterUniversity of Aveiro, Campus Universitário de SantiagoAveiroPortugal

Personalised recommendations