Skip to main content
SpringerLink
Log in

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

  • Research Article
  • Published:
Experimental Brain Research Aims and scope Submit manuscript

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Notes

  1. The terms “M-displacement” and “forward displacement” will be used, in the present paper, interchangeably and will be reserved for the empirically observed localization errors, with RM and RG referring to theoretical constructs hypothesized to modulated the latter, biasing the perceived offset forward, in the direction of (seen) motion, and downward, in the direction of (perceived) gravity, respectively.

References

  • 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 12:569–582

    CAS  Google Scholar 

  • Ashida H (2004) Action-specific extrapolation of target motion in human visual system. Neuropsychologia 42:1515–1524

    PubMed  Google Scholar 

  • Barton JJ, Sharpe JA, Raymond JE (1996) Directional defects in pursuit and motion perception in humans with unilateral cerebral lesions. Brain 119:1535–1550

    PubMed  Google Scholar 

  • Bertamini M (1993) Memory for position and dynamic representations. Mem Cognit 21:449–457

    CAS  PubMed  Google Scholar 

  • Born RT, Bradley DC (2005) Structure and function of visual area MT. Ann Rev Neurosci 28:157–189

    CAS  PubMed  Google Scholar 

  • 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 28:12071–12084

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bosco G, Delle Monache S, Lacquaniti F (2012) Catching what we cannot see: manual interception of occluded fly-ball trajectories. PLoS One 7:e49381

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 23:9–13

    Google Scholar 

  • Collewijn H, Tamminga EP (1984) Human smooth pursuit and saccadic eye movements during voluntary pursuit of different motions on different backgrounds. J Physiol (London) 351:217–250

    CAS  Google Scholar 

  • Corbetta N, Shulman G (2002) Control of goal-directed and stimulus-driven attention in the brain. Nat Rev Neurosci 3(3):201–215

    CAS  PubMed  Google Scholar 

  • Corbetta M, Patel G, Shulman G (2008) The reorienting system of the human brain: from environment to theory of mind. Neuron 58:306–354

    CAS  PubMed  PubMed Central  Google Scholar 

  • De Sá Teixeira NA (2014) Fourier decomposition of spatial localization errors reveals an idiotropic dominance of an internal model of gravity. Vision Res 105:177–188

    PubMed  Google Scholar 

  • 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):2491–2504

    PubMed  Google Scholar 

  • De Sá Teixeira NA, Hecht H (2014) Can representational trajectory reveal the nature of an internal model of gravity? Atten Percept Psychophys 76:1106–1120

    PubMed  Google Scholar 

  • De Sá Teixeira NA, Hecht H, Oliveira AM (2013) The representational dynamics of remembered projectile locations. J Exp Psychol Hum Percept Perform 39:1690–1699

    PubMed  Google Scholar 

  • 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)

    PubMed  Google Scholar 

  • 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):359–374

    PubMed  Google Scholar 

  • 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):1809–1823

    PubMed  PubMed Central  Google Scholar 

  • 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 114:2983–2990

    CAS  PubMed  PubMed Central  Google Scholar 

  • Freyd JJ (1983) The mental representation of movement when static stimuli are viewed. Percept Psychophys 33:575–581

    CAS  PubMed  Google Scholar 

  • Freyd JJ, Finke RA (1984) Representational momentum. J Exp Psychol Learn Mem Cogn 10:126–132

    Google Scholar 

  • Freyd JJ, Finke RA (1985) A velocity effect for representational momentum. Bull Psychono Soc 23:443–446

    Google Scholar 

  • Freyd JJ, Johnson JQ (1987) Probing the time course of representational momentum. J Exp Psychol Learn Mem Cogn 13:259–269

    CAS  PubMed  Google Scholar 

  • Freyd JJ, Miller GF (1992) Creature motion. Bull Psychon Soc 30(6):470

    Google Scholar 

  • 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 181–204

    Google Scholar 

  • Freyd JJ, Pantzer TM, Cheng JL (1988) Representing statics as forces in equilibrium. J Exp Psychol Gen 117:395–407

    CAS  PubMed  Google Scholar 

  • Freyd JJ, Kelly MH, DeKay ML (1990) Representational momentum in memory for pitch. J Exp Psychol Learn Mem Cogn 16:1107–1117

    CAS  PubMed  Google Scholar 

  • Getzmann S, Lewald J, Guski R (2004) Representational momentum in spatial hearing. Perception 33:591–599

    PubMed  Google Scholar 

  • Hayes AE, Freyd JJ (2002) Representational momentum when attention is divided. Vis Cognit 9:8–27

    Google Scholar 

  • Huang ZY, Edwards MJ, Rounis E, Bhatia KP, Rothwell JC (2005) Theta burst stimulation of the human motor cortex. Neuron 45(2):201–206

    CAS  PubMed  Google Scholar 

  • Hubbard TL (1990) Cognitive representation of linear motion: possible direction and gravity effects in judged displacement. Mem Cognit 18:299–309

    CAS  PubMed  Google Scholar 

  • Hubbard TL (2005) Representational momentum and related displacements in spatial memory: a review of the findings. Psychon Bull Rev 12:822–851

    PubMed  Google Scholar 

  • Hubbard TL (2006) Computational theory and cognition in representational momentum and related types of displacement: a reply to Kerzel. Psychon Bull Rev 13:174–177

    Google Scholar 

  • 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 338–365

    Google Scholar 

  • Hubbard TL (2014) Forms of momentum across space: representational, operational, and attentional. Psychon Bull Rev 21:1371–1403

    PubMed  Google Scholar 

  • Hubbard TL (2015) Forms of momentum across time: behavioral and psychological. J Mind Behav 36:47–82

    Google Scholar 

  • Hubbard TL, Bharucha JJ (1988) Judged displacement in apparent vertical and horizontal motion. Percept Psychophys 44:211–221

    CAS  PubMed  Google Scholar 

  • Hubbard TL, Ruppel SE (2002) A possible role of naïve impetus in Michotte’s “launching effect”: evidence from representational momentum. Vis Cognit 9:153–176

    Google Scholar 

  • Indovina I, Maffei V, Bosco G, Zago M, Macaluso E, Lacquaniti F (2005) Representation of visual gravitational motion in the human vestibular cortex. Science 308:416–419

    CAS  PubMed  Google Scholar 

  • 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 71:114–124

    PubMed  Google Scholar 

  • 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):2365–2371

    PubMed  Google Scholar 

  • Jörges B, López-Moliner J (2017) Gravity as a strong prior: implications for perception and action. Front Hum Neurosci 11:203

    PubMed  PubMed Central  Google Scholar 

  • Kelly MH, Freyd JJ (1987) Explorations of representational momentum. Cognit Psychol 19:369–401

    CAS  PubMed  Google Scholar 

  • Kerzel D (2000) Eye movements and visible persistence explain the mislocalization of the final position of a moving target. Vis Res 40:3703–3715

    CAS  PubMed  Google Scholar 

  • Kerzel D (2002) The locus of “memory displacement” is at least partially perceptual: effects of velocity, expectation, friction, memory averaging, and weight. Percept Psychophys 64:680–692

    PubMed  Google Scholar 

  • Kerzel D (2003a) Mental extrapolation of target position is strongest with weak motion signals and motor responses. Vis Res 43:2623–2635

    PubMed  Google Scholar 

  • Kerzel D (2003b) Attention maintains mental extrapolation of target position: irrelevant distractors eliminate forward displacement after implied motion. Cognition 88:109–131

    PubMed  Google Scholar 

  • Kerzel D (2003c) Centripetal force draws the eyes, not memory of the target, toward the center. J Exp Psychol Learn Mem Cogn 29:458–466

    PubMed  Google Scholar 

  • Kerzel D (2004) Attentional load modulates mislocalization of moving stimuli, but does not eliminate the error. Psychon Bull Rev 11(5):848–853

    PubMed  Google Scholar 

  • Kerzel D (2006) Why eye movements and perceptual factors have to be controlled in studies on “Representational Momentum”. Psychol Bull Rev 13:166–173

    Google Scholar 

  • Kerzel D, Gegenfurtner KR (2003) Neuronal processing delays are compensated in the sensorimotor branch of the visual system. Curr Biol 13:1975–1978

    CAS  PubMed  Google Scholar 

  • 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 27:829–840

    CAS  PubMed  Google Scholar 

  • Kourtzi Z, Kanwisher N (2000) Activation in human MT/MST for static images with implied motion. J Cognit Neurosci 12:48–55

    CAS  Google Scholar 

  • La Scaleia B, Lacquaniti F, Zago M (2014) Neural extrapolation of motion for a ball rolling down an inclined plane. PLoS One 9:e99837

    PubMed  PubMed Central  Google Scholar 

  • 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 114:1577–1592

    PubMed  PubMed Central  Google Scholar 

  • Lacquaniti F, Maioli C (1987) Anticipatory and reflex coactivation of antagonistic muscles in catching. Brain Res 406(1–2):373–378

    CAS  PubMed  Google Scholar 

  • Lacquaniti F, Maioli C (1989) The role of preparation in tuning anticipatory and reflex responses during catching. J Neurosci 9(1):134–148

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 7:101

    Google Scholar 

  • 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. https://doi.org/10.1155/2014/615854

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 28:397–426

    PubMed  Google Scholar 

  • Lopez C, Blanke O, Mast FW (2012) The human vestibular cortex revealed by coordinate-based activation likelihood estimation meta-analysis. Neuroscience 212:159–179

    CAS  PubMed  Google Scholar 

  • Luebke AE, Robinson DA (1988) Transition dynamics between pursuit and fixation suggest different systems. Vision Res 28:941–946

    CAS  PubMed  Google Scholar 

  • 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):127

    Google Scholar 

  • 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 78:55–69

    PubMed  Google Scholar 

  • McGeorge P, Beschin N, Della Sala S (2006) Representing target motion: the role of the right hemispehre in the forward displacement bias. Neuropsychology 20:708–715

    PubMed  Google Scholar 

  • McIntyre J, Zago M, Berthoz A, Lacquaniti F (2001) Does the brain model Newton’s laws? Nat Neurosci 4:693–694

    CAS  PubMed  Google Scholar 

  • Missal M, Heinin SJ (2017) Stopping smooth pursuit. Philos Trans R Soc B 372:20160200

    Google Scholar 

  • Mitrani L, Dimitrov G (1978) Pursuit eye movements of a disappearing moving target. Vision Res 18:537–539

    CAS  PubMed  Google Scholar 

  • Moscatelli A, Lacquaniti F (2011) The weight of time: gravitational force enhances discrimination of visual motion duration. J Vis 11(4):1–17

    Google Scholar 

  • 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):1076–1083

    PubMed  Google Scholar 

  • Müsseler J, Stork S, Kerzel D (2002) Comparing mislocalizations with moving stimuli: the Fröhlich effect, the flash-lag, and representational momentum. Vis Cognit 9:120–138

    Google Scholar 

  • Nagai M, Kazai K, Yagi A (2002) Larger forward memory displacement in the direction of gravity. Vis Cognit 9:28–40

    Google Scholar 

  • 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 41:1757–1768

    PubMed  Google Scholar 

  • Pola J, Wyatt HJ (1997) Offset dynamics of human smooth pursuit eye movements: effects of target presence and subject attention. Vis Res 37(18):2579–2595

    CAS  PubMed  Google Scholar 

  • 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 23:98–103

    PubMed  Google Scholar 

  • Reed CL, Vinson NG (1996) Conceptual effects on representational momentum. J Exp Psychol Hum Percept Perform 22:839–850

    CAS  PubMed  Google Scholar 

  • Ridding MC, Ziemann U (2010) Determinants of the induction of cortical plasticity by non-invasive brain stimulation in healthy subjects. J Physiol 588:2291–2304

    CAS  PubMed  PubMed Central  Google Scholar 

  • Riečanskỳ I (2004) Extrastriate area V5 (MT) and its role in the processing of visual motion. Ceskoslovenka Fysiologie 53(1):17–22

    Google Scholar 

  • 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):1071–1107

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 36:2189–2195

    CAS  PubMed  Google Scholar 

  • 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 6:7544

    PubMed  Google Scholar 

  • 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 5:15–38

    CAS  Google Scholar 

  • Sekuler R, Armstrong R (1978) Fourier analysis of polar coordinate data in visual physiology and psychophysics. Behav Res Methods Instrum 10:8–14

    Google Scholar 

  • 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):s887

    Google Scholar 

  • Senior C, Ward J, David AS (2002) Representational momentum and the brain: an investigation into the functional necessity of V5/MT. Vis Cognit 9:81–92

    Google Scholar 

  • 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):8445–8456

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sestieri C, Shulman GL, Corbetta M (2017) The contribution of the human posterior parietal cortex to episodic memory. Nat Rev Neurosci 18(3):183–192

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sunaert S, Van Hecke P, Marchal G, Orban GA (1999) Motion-responsive regions of the human brain. Exp Brain Res 127(4):355–370

    CAS  PubMed  Google Scholar 

  • 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 87:2700–2714

    PubMed  Google Scholar 

  • 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 87:802–818

    PubMed  Google Scholar 

  • 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):443–459

    PubMed  PubMed Central  Google Scholar 

  • Vinson NG, Reed CL (2002) Sources of object-specific effects in representational momentum. Vis Cognit 9:41–65

    Google Scholar 

  • 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):1–16

    Google Scholar 

  • White H, Minor SW, Merrell J, Smith T (1993) Representational-momentum effects in the cerebral hemispheres. Brain Cognit 22:161–170

    CAS  Google Scholar 

  • Wischnewski M, Schutter DJLG (2015) Efficacy and time course of theta burst stimulation in healthy humans. Brain Stimul 8(4):685–692

    PubMed  Google Scholar 

  • Zago M, Lacquaniti F (2005) Cognitive, perceptual and action-oriented representations of falling objects. Neuropsychologia 43(2):178–188

    PubMed  Google Scholar 

  • Zeki S (2015) Area V5—a microcosm of the visual brain. Front Integ Neurosci 9:21

    Google Scholar 

Download references

Acknowledgements

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).

Author information

Authors and Affiliations

  1. Department of Systems Medicine and Centre of Space Biomedicine, University of Rome ‘Tor Vergata’, 00133, Rome, Italy

    Nuno Alexandre De Sá Teixeira, Gianfranco Bosco, Sergio Delle Monache & Francesco Lacquaniti

  2. Laboratory of Neuromotor Physiology, IRCCS Santa Lucia Foundation, 00179, Rome, Italy

    Nuno Alexandre De Sá Teixeira, Gianfranco Bosco, Sergio Delle Monache & Francesco Lacquaniti

  3. Department of Education and Psychology, William James Research Center, University of Aveiro, Campus Universitário de Santiago, 3810-193, Aveiro, Portugal

    Nuno Alexandre De Sá Teixeira

Authors
  1. Nuno Alexandre De Sá Teixeira
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Gianfranco Bosco
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Sergio Delle Monache
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Francesco Lacquaniti
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Nuno Alexandre De Sá Teixeira.

Additional information

Communicated by Melvyn A. Goodale.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

De Sá Teixeira, N.A., Bosco, G., Delle Monache, S. et al. The role of cortical areas hMT/V5+ and TPJ on the magnitude of representational momentum and representational gravity: a transcranial magnetic stimulation study. Exp Brain Res 237, 3375–3390 (2019). https://doi.org/10.1007/s00221-019-05683-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00221-019-05683-z

Keywords

Search

Navigation