Skip to main content
SpringerLink
Log in

fMR-adaptation reveals separate processing regions for the perception of form and texture in the human ventral stream

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

Abstract

We recently demonstrated that attending to the form of objects and attending to their surface properties activated anatomically distinct regions of occipito-temporal cortex (Cant and Goodale, Cereb Cortex 17:713–731, 2007). Specifically, attending to form activated the lateral occipital area (LO), whereas attending to texture activated the collateral sulcus (CoS). Although these regions showed preferential activation to one particular stimulus dimension (e.g. texture in CoS), they also showed activation to other, non-preferred stimulus dimensions (e.g. form in CoS). This raises the question as to whether the activation associated with attention to form in CoS, for example, represents the actual processing of object form or instead represents the obligatory processing of object texture that occurred when people attended to form. To investigate this, we conducted an fMR-adaptation experiment which allowed us to examine the response properties of regions specialized for processing form, texture, and colour when participants were not explicitly attending to a particular stimulus dimension. Participants passively viewed blocks where only one dimension varied and blocks where no dimensions varied, while fixating a cross in the centre of the display. Area LO was most sensitive to variations in form, whereas the CoS was most sensitive to variations in texture. As in our previous study, no regions were found that were most sensitive to variations in colour, but unlike the results from that study, medial regions of the ventral stream along the fusiform gyrus and CoS showed some selectivity to colour. Taken together, these results replicate the findings from our previous study and provide additional evidence for the existence of separate processing pathways for form and surface properties (particularly texture) in the ventral stream.

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

Similar content being viewed by others

References

  • Anderson RA, Brotchie PR, Mazzoni P (1992) Evidence for the lateral intraparietal area as the parietal eye field. Curr Opin Neurobiol 2:840–846

    Article  Google Scholar 

  • Andrews TJ, Ewbank MP (2004) Distinct representations for facial identity and changeable aspects of faces in the human temporal lobe. Neuroimage 23:905–913

    Article  PubMed  Google Scholar 

  • Arnott SR, Cant JS, Dutton GN, Goodale MA (2008) Crinkling and crumpling: an auditory fMRI study of material properties. Neuroimage (in press)

  • Bar M, Tootell RBH, Schacter DL, Greve DN, Fischl B, Mendola JD, Rosen BR, Dale AM (2001) Cortical mechanisms specific to explicit visual object recognition. Neuron 29:529–535

    Article  PubMed  CAS  Google Scholar 

  • Beauchamp MS, Haxby JV, Jennings JE, DeYoe EA (1999) An fMRI version of the Farnsworth-Munsell 100-Hue test reveals multiple color-selective areas in human ventral occipitotemporal cortex. Cereb Cortex 9:257–263

    Article  PubMed  CAS  Google Scholar 

  • Bursztyn LL, Ganesh G, Imamizu H, Kawato M, Flanagan JR (2006) Neural correlates of internal-model loading. Curr Biol 16:2440–2445

    Article  PubMed  CAS  Google Scholar 

  • Cant JS, Goodale MA (2007) Attention to form or surface properties modulates different regions of human occipitotemporal cortex. Cereb Cortex 17:713–731

    Article  PubMed  Google Scholar 

  • Cant JS, Large M-E, McCall L, Goodale MA (2008) Independent processing of form, colour, and texture in object perception. Perception 37:57–78

    Article  PubMed  Google Scholar 

  • Cavina-Pratesi C, Goodale MA, Culham JC (2007) fMRI reveals a dissociation between grasping and perceiving the size of real 3D objects. PLoS One 2:e424

    Article  PubMed  Google Scholar 

  • Colby CL, Duhamel JR, Goldberg ME (1996) Visual, presaccadic, and cognitive activation of single neurons in monkey lateral intraparietal area. J Neurophysiol 76:2841–2852

    PubMed  CAS  Google Scholar 

  • Corbetta M, Miezin FM, Dobmeyer S, Shulman GL, Petersen SE (1990) Attentional modulation of neural processing of shape, color, and velocity in humans. Science 248:1556–1559

    Article  PubMed  CAS  Google Scholar 

  • Corbetta M, Miezin FM, Dobmeyer S, Shulman GL, Petersen SE (1991) Selected and divided attention during visual discrimination of shape, color, and speed: functional anatomy by positron emission tomography. J Neurosci 11:2383–2402

    PubMed  CAS  Google Scholar 

  • Cox RW (1996) AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. Comput Biomed Res 29:162–173

    Article  PubMed  CAS  Google Scholar 

  • Culham JC (2006) Functional neuroimaging: experimental design and analysis. In: Cabeza R, Kingstone A (eds) Handbook of functional neuroimaging of cognition, 2nd edn. MIT Press, Cambridge, pp 53–82

    Google Scholar 

  • Culham JC, Kanwisher NG (2001) Neuroimaging of cognitive functions in human parietal cortex. Curr Opin Neurobiol 11:157–163

    Article  PubMed  CAS  Google Scholar 

  • Davare M, Andres M, Clerget E, Thonnard J-L, Olivier E (2007) Temporal dissociation between hand shaping and grip force scaling in the anterior intraparietal area. J Neurosci 27:3974–3980

    Article  PubMed  CAS  Google Scholar 

  • Desimone R, Schein SJ (1987) Visual properties of neurons in area V4 of the macaque: sensitivity to stimulus form. J Neurophysiol 57:835–868

    PubMed  CAS  Google Scholar 

  • Duvelleroy-Hommet C, Gillet P, Cottier JP, de Toffol B, Saudeau D, Corcia P, Autret A (1997) Cerebral achromatopsia without prosopagnosia, alexia, object agnosia. Rev Neurol (Paris) 153:554–560

    CAS  Google Scholar 

  • Ehrsson HH, Fagergren A, Jonsson T, Westling G, Johansson RS, Forssberg H (2000) Cortical activity in precision-versus power-grip tasks: an fMRI study. J Neurophysiol 83:528–536

    PubMed  CAS  Google Scholar 

  • Ehrsson HH, Fagergren A, Forssberg H (2001) Differential fronto-parietal activation depending on force used in a precision task: an fMRI study. J Neurophysiol 85:2613–2623

    PubMed  CAS  Google Scholar 

  • Epstein R, Kanwisher N (1998) A cortical representation of the local visual environment. Nature 392:598–601

    Article  PubMed  CAS  Google Scholar 

  • Ewbank MP, Schluppeck D, Andrews TJ (2005) fMR-adaptation reveals a distributed representation of inanimate objects and places in human visual cortex. Neuroimage 28:268–279

    Article  PubMed  Google Scholar 

  • Freire L, Mangin JF (2001) Motion correction algorithms may create spurious brain activations in the absence of subject motion. Neuroimage 14:709–722

    Article  PubMed  CAS  Google Scholar 

  • Friston KJ, Homes AP, Worsley KJ, Poline J-P, Frith CD, Frackwowiak RSJ (1995) Statistical parametric maps in functional imaging: a general linear model approach. Hum Brain Mapp 2:189–210

    Article  Google Scholar 

  • Garner WR (1974) The processing of information and structure. Erlbaum, Potomac

    Google Scholar 

  • Grady CL, Maisog JM, Horwitz B, Ungerleider LG, Mentis MJ, Salerno JA, Pietrini P, Wagner E, Haxby JV (1994) Age-related changes in cortical blood flow activation during visual processing of faces and location. J Neurosci 14:1450–1462

    PubMed  CAS  Google Scholar 

  • Grill-Spector K, Henson R, Martin A (2006) Repetition and the brain: neural models of stimulus-specific effects. Trends Cogn Sci 10:14–23

    Article  PubMed  Google Scholar 

  • Grill-Spector K, Kourtzi Z, Kanwisher N (2001) The lateral occipital complex and its role in object recognition. Vision Res 41:1409–1422

    Article  PubMed  CAS  Google Scholar 

  • Grill-Spector K, Kushnir T, Edelman S, Avidan G, Itzchak Y, Malach R (1999) Differential processing of objects under various viewing conditions in the human lateral occipital complex. Neuron 24:187–203

    Article  PubMed  CAS  Google Scholar 

  • Grill-Spector K, Kushnir T, Edelman S, Itzchak Y, Malach R (1998) Cue-invariant activation in object-related areas of the human occipital lobe. Neuron 21:191–202

    Article  PubMed  CAS  Google Scholar 

  • Grill-Spector K, Malach R (2001) fMR-adaptation: a tool for studying the functional properties of human cortical neurons. Acta Psychol 107:293–321

    Article  CAS  Google Scholar 

  • Grill-Spector K, Malach R (2004) The human visual cortex. Annu Rev Neurosci 27:649–677

    Article  PubMed  CAS  Google Scholar 

  • Goodale MA, Milner AD (2004) Sight unseen: an exploration of conscious and unconscious vision. Oxford University Press, Oxford

    Google Scholar 

  • Gordon AM, Westling G, Cole KJ, Johansson RS (1993) Memory representations underlying motor commands used during manipulation of common and novel objects. J Neurophysiol 69:1789–1796

    PubMed  CAS  Google Scholar 

  • Hadjikhani N, Liu AK, Dale AM, Cavanagh P, Tootell RBH (1998) Retinotopy and color sensitivity in human visual cortical area V8. Nat Neurosci 1:235–241

    Article  PubMed  CAS  Google Scholar 

  • Hanazawa A, Komatsu H (2001) Influence of the direction of elemental luminance gradients on the responses of V4 cells to textured surfaces. J Neurosci 21:4490–4497

    PubMed  CAS  Google Scholar 

  • Hasson U, Harel M, Levy I, Malach R (2003) Large-scale mirror-symmetry organization of human occipito-temporal object areas. Neuron 37:1027–1041

    Article  PubMed  CAS  Google Scholar 

  • Haxby JV, Gobbini MI, Furey ML, Ishai A, Schouten JL, Pietrini P (2001) Distributed and overlapping representations of faces and objects in ventral temporal cortex. Science 293:2425–2430

    Article  PubMed  CAS  Google Scholar 

  • Haxby JV, Horwitz B, Ungerleider LG, Maisog JM, Pietrini P, Grady CL (1994) The functional organization of human extrastriate cortex: a PET-rCBF study of selective attention to faces and locations. J Neurosci 14:6336–6353

    PubMed  CAS  Google Scholar 

  • Hayworth K, Biederman I (2006) Neural evidence for intermediate representations in object recognition. Vision Res 46:4024–4031

    Article  PubMed  Google Scholar 

  • Henson RN (2003) Neuroimaging studies of priming. Prog Neurobiol 70:53–81

    Article  PubMed  CAS  Google Scholar 

  • Heywood CA, Cowey A (1987) On the role of cortical area V4 in the discrimination of hue and pattern in macaque monkeys. J Neurosci 7:2601–2617

    PubMed  CAS  Google Scholar 

  • Heywood CA, Gaffan D, Cowey A (1995) Cerebral achromatopsia in monkeys. Eur J NeuroSci 7:1064–1073

    Article  PubMed  CAS  Google Scholar 

  • Heywood CA, Kentridge RW (2003) Achromatopsia, color vision, and cortex. Neurol Clin 21:483–500

    Article  PubMed  Google Scholar 

  • Humphrey GK, Goodale MA, Jakobson LS, Servos P (1994) The role of surface information in object recognition: studies of a visual form agnosic and normal subjects. Perception 23:1457–1481

    Article  PubMed  CAS  Google Scholar 

  • Imamizu H, Kuroda T, Yoshioka T, Kawato M (2004) Functional magnetic resonance imaging examination of two modular architectures for switching multiple internal models. J Neurosci 24:1173–1181

    Article  PubMed  CAS  Google Scholar 

  • James TW, Culham J, Humphrey GK, Milner AD, Goodale MA (2003) Ventral occipital lesions impair object recognition but not object-directed grasping: an fMRI study. Brain 126:2463–2475

    Article  PubMed  Google Scholar 

  • James TW, Humphrey GK, Gati JS, Menon RS, Goodale MA (2002) Differential effects of viewpoint on object-driven activation in dorsal and ventral streams. Neuron 35:793–801

    Article  PubMed  CAS  Google Scholar 

  • Kanwisher NG, Chun MM, McDermott J, Ledden PJ (1996) Functional imaging of human visual recognition. Cogn Brain Res 5:55–67

    Article  CAS  Google Scholar 

  • Kanwisher N, McDermott J, Chun M (1997) The fusiform face area: a module in human extrastriate cortex specialized for face perception. J Neurosci 17:4302–4311

    PubMed  CAS  Google Scholar 

  • Kastner S, De Weerd P, Ungerleider LG (2000) Texture segregation in the human visual cortex: a functional MRI study. J Neurophysiol 83:2453–2457

    PubMed  CAS  Google Scholar 

  • Kourtzi Z, Kanwisher N (2000) Cortical regions involved in perceiving object shape. J Neurosci 20:331–3318

    Google Scholar 

  • Kourtzi Z, Kanwisher N (2001) Representation of perceived object shape by the human lateral occipital complex. Science 293:1506–1509

    Article  PubMed  CAS  Google Scholar 

  • Kroliczak G, Cavina-Pratesi C, Goodman DA, Culham JC (2007) What does the brain do when you fake it? An fMRI study of pantomimed and real grasping. J Neurophysiol 97:2410–2422

    Article  PubMed  CAS  Google Scholar 

  • Kuhtz-Buschbeck JP, Ehrsson HH, Forssberg H (2001) Human brain activity in the control of fine static precision grip forces: an fMRI study. Eur J Neurosci 14:382–390

    Article  PubMed  CAS  Google Scholar 

  • Levy I, Hasson U, Avidan G, Hendler T, Malach R (2001) Center-periphery organization of human object areas. Nat Neurosci 4:533–539

    PubMed  CAS  Google Scholar 

  • Lueck CJ, Zeki S, Friston KJ, Deiber MP, Cope P, Cunningham VJ, Lammerstma AA, Kennard C, Frackowiak RSJ (1989) The colour centre in the cerebral cortex of man. Nature 340:386–388

    Article  PubMed  CAS  Google Scholar 

  • Malach R, Reppas JB, Benson RR, Kwong KK, Jiang H, Kennedy WA, Ledden PJ, Brady TJ, Rosen BR, Tootell RB (1995) Object-related activity revealed by functional magnetic resonance imaging in human occipital cortex. Proc Natl Acad Sci USA 92:8135–8139

    Article  PubMed  CAS  Google Scholar 

  • McKeefry DJ, Zeki S (1997) The position and topography of the human colour centre as revealed by functional magnetic resonance imaging. Brain 120:2229–2242

    Article  PubMed  Google Scholar 

  • Miceli G, Fouch E, Capasso R, Shelton JR, Tomaiuolo F, Caramazza A (2001) The dissociation of color from form and function knowledge. Nat Neurosci 4:662–667

    Article  PubMed  CAS  Google Scholar 

  • Milner AD, Perrett DI, Johnston RS, Benson PJ, Jordan TR, Heeley DW, Bettucci D, Mortara F, Mutani R, Terazzi E (1991) Perception and action in ‘visual form agnosia’. Brain 114:405–428

    Article  PubMed  Google Scholar 

  • Murray SO, Wojciulik E (2004) Attention increases neural selectivity in the human lateral occipital complex. Nat Neurosci 7:70–74

    Article  PubMed  CAS  Google Scholar 

  • Ogawa S, Tank DW, Menon R, Ellermann JM, Kim SG, Merkle H, Ugurbil K (1992) Intrinsic signal changes accompanying sensory stimulation: functional brain mapping with magnetic resonance imaging. Proc Natl Acad Sci USA 89:5951–5955

    Article  PubMed  CAS  Google Scholar 

  • Peuskens H, Claeys KG, Todd JT, Norman JF, Van Hecke P, Orban GA (2004) Attention to 3-D shape, 3-D motion, and texture in 3-D structure from motion displays. J Cogn Neurosci 16:665–682

    Article  PubMed  Google Scholar 

  • Price CJ, Humphreys GW (1989) The effects of surface detail on object categorization and naming. Q J Exp Psychol 41A:797–827

    Google Scholar 

  • Puce A, Allison T, Asgari M, Gore JC, McCarthy G (1996) Differential sensitivity of human visual cortex to faces, letterstrings, and textures: a functional magnetic resonance imaging study. J Neurosci 16:5205–5215

    PubMed  CAS  Google Scholar 

  • Reddy L, Kanwisher N (2006) Coding of visual objects in the ventral stream. Curr Opin Neurobiol 16:408–414

    Article  PubMed  CAS  Google Scholar 

  • Russell R, Sinha P, Biederman I, Nederhouser M (2006) Is pigmentation important for face recognition? Evidence from contrast negation. Perception 35:749–759

    Article  PubMed  Google Scholar 

  • Schacter DL, Buckner RL (1998) Priming and the brain. Neuron 20:185–195

    Article  PubMed  CAS  Google Scholar 

  • Sergent J, Ohta S, MacDonald B (1992) Functional neuroanatomy of face and object processing. Brain 115:15–36

    Article  PubMed  Google Scholar 

  • Steeves JKE, Humphrey GK, Culham JC, Menon RS, Milner AD, Goodale MA (2004) Behavioral and neuroimaging evidence for a contribution of color and texture information to scene classification in a patient with visual form agnosia. J Cogn Neurosci 16:1–11

    Article  Google Scholar 

  • Talairach J, Tournoux P (1988) Co-planar stereotaxic atlas of the human brain. Thieme Medical Publishers, New York

    Google Scholar 

  • Tarr MJ, Kersten D, Cheng Y, Doerschner K, Rossion B (2002) Men are from mars, women are from venus: behavioral and neural correlates of face sexing using color. J Vision 2:598a

    Article  Google Scholar 

  • Tarr MJ, Kersten D, Cheng Y, Rossion B (2001) It’s pat! Sexing faces using only red and green. J Vision 1:337a

    Google Scholar 

  • Tootell RBH, Tsao D, Vanduffel W (2003) Neuroimaging weighs in: humans meet macaques in “primate” visual cortex. J Neurosci 23:3981–3989

    PubMed  CAS  Google Scholar 

  • Valyear KF, Culham JC, Sharif N, Westwood D, Goodale MA (2006) A double dissociation between sensitivity to changes in object identity and object orientation in the ventral and dorsal visual streams: a human fMRI study. Neurophysiology 44:218–228

    Google Scholar 

  • Vandenberghe R, Price C, Wise R, Josephs O, Frackowiak RSJ (1996) Functional anatomy of a common semantic system for words and pictures. Nature 383:254–256

    Article  PubMed  CAS  Google Scholar 

  • Wiggs CL, Martin A (1998) Properties and mechanisms of perceptual priming. Curr Opin Neurobiol 8:227–233

    Article  PubMed  CAS  Google Scholar 

  • Wilson HR, Loffler G, Wilkinson F (2002) Synthetic faces, face cubes, and the geometry of face space. Vision Res 42:2909–2923

    Article  PubMed  Google Scholar 

  • Xu Y, Turk-Browne NB, Chun MM (2007) Dissociating task performance from fMRI repetition attenuation in ventral visual cortex. J Neurosci 27:5981–5985

    Article  PubMed  CAS  Google Scholar 

  • Zeki SM (1973) Colour coding in rhesus monkey prestriate cortex. Brain Res 53:422–427

    Article  PubMed  CAS  Google Scholar 

  • Zeki S, Aglioti S, McKeefry D, Berlucchi G (1999) The neurological basis of conscious color perception in a blind patient. Proc Natl Acad Sci USA 96:14124–14129

    Article  PubMed  CAS  Google Scholar 

  • Zeki S, Watson JDG, Lueck CJ, Friston KJ, Kennard C, Frackowiak RSJ (1991) A direct demonstration of functional specialization in human visual cortex. J Neurosci 11:641–649

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This research was supported by the Canadian Institutes of Health Research (MAG, SRA) and the Canada Research Chairs Program (MAG) and a postgraduate scholarship from the Natural Sciences and Engineering Research Council of Canada (JSC).

Author information

Authors and Affiliations

  1. CIHR Group on Action and Perception, University of Western Ontario, London, ON, Canada

    Jonathan S. Cant, Stephen R. Arnott & Melvyn A. Goodale

  2. Neuroscience Program, University of Western Ontario, London, ON, Canada

    Jonathan S. Cant & Melvyn A. Goodale

  3. Department of Psychology, University of Western Ontario, London, ON, N6A 5C2, Canada

    Jonathan S. Cant, Stephen R. Arnott & Melvyn A. Goodale

Authors
  1. Jonathan S. Cant
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Stephen R. Arnott
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Melvyn A. Goodale
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Melvyn A. Goodale.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Cite this article

Cant, J.S., Arnott, S.R. & Goodale, M.A. fMR-adaptation reveals separate processing regions for the perception of form and texture in the human ventral stream. Exp Brain Res 192, 391–405 (2009). https://doi.org/10.1007/s00221-008-1573-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00221-008-1573-8

Keywords

Search

Navigation