IDEAS home Printed from https://ideas.repec.org/a/plo/pbio00/0060187.html
   My bibliography  Save this article

Multivariate Patterns in Object-Selective Cortex Dissociate Perceptual and Physical Shape Similarity

Author

Listed:
  • Johannes Haushofer
  • Margaret S Livingstone
  • Nancy Kanwisher

Abstract

Prior research has identified the lateral occipital complex (LOC) as a critical cortical region for the representation of object shape in humans. However, little is known about the nature of the representations contained in the LOC and their relationship to the perceptual experience of shape. We used human functional MRI to measure the physical, behavioral, and neural similarity between pairs of novel shapes to ask whether the representations of shape contained in subregions of the LOC more closely reflect the physical stimuli themselves, or the perceptual experience of those stimuli. Perceptual similarity measures for each pair of shapes were obtained from a psychophysical same-different task; physical similarity measures were based on stimulus parameters; and neural similarity measures were obtained from multivoxel pattern analysis methods applied to anterior LOC (pFs) and posterior LOC (LO). We found that the pattern of pairwise shape similarities in LO most closely matched physical shape similarities, whereas shape similarities in pFs most closely matched perceptual shape similarities. Further, shape representations were similar across participants in LO but highly variable across participants in pFs. Together, these findings indicate that activation patterns in subregions of object-selective cortex encode objects according to a hierarchy, with stimulus-based representations in posterior regions and subjective and observer-specific representations in anterior regions. : As early as 1031 a.d., the Arab scholar Ibn al-Haytham suggested that visual experience was not veridical, but inherently subjective. During the last few decades, this observation has given rise to one of the core questions in visual neuroscience: how does the subjective experience of visual stimuli relate to their neural representations in the brain? It is well-known that visual shape is represented in a brain region called lateral occipital complex (LOC). However, do these representations reflect physical or perceptual stimulus characteristics? We presented observers with a set of complex visual stimuli and obtained three measures of similarity for these stimuli: a physical similarity measure based on stimulus parameters; a behavioral similarity measure based on discrimination performance; and finally a neural similarity measure based on multivariate pattern analyses in LOC. We found that in anterior LOC, neural stimulus similarities correlated with subjective perceptual similarities, but not with physical stimulus similarities; the reverse was true in posterior LOC. In addition, neural similarities were consistent across participants in posterior LOC, but highly variable across participants in anterior LOC. Together these findings suggest a two-part answer to the question of how cortical object representations relate to subjective experience: anterior regions appear to contain subjective, individually variable shape representations, whereas posterior regions contain stimulus-based shape representations. How does the subjective experience of visual shapes relate to the neural representations of these shapes in the brain? Using psychophysics, functional MRI, and multivariate pattern analysis methods, this study shows that activation patterns in anterior, shape-selective brain regions reflect perceptual shape similarities, whereas patterns in posterior regions reflect physical similarities.

Suggested Citation

  • Johannes Haushofer & Margaret S Livingstone & Nancy Kanwisher, 2008. "Multivariate Patterns in Object-Selective Cortex Dissociate Perceptual and Physical Shape Similarity," PLOS Biology, Public Library of Science, vol. 6(7), pages 1-9, July.
  • Handle: RePEc:plo:pbio00:0060187
    DOI: 10.1371/journal.pbio.0060187
    as

    Download full text from publisher

    File URL: https://journals.plos.org/plosbiology/article?id=10.1371/journal.pbio.0060187
    Download Restriction: no

    File URL: https://journals.plos.org/plosbiology/article/file?id=10.1371/journal.pbio.0060187&type=printable
    Download Restriction: no

    File URL: https://libkey.io/10.1371/journal.pbio.0060187?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Nikos K. Logothetis & Jon Pauls & Mark Augath & Torsten Trinath & Axel Oeltermann, 2001. "Neurophysiological investigation of the basis of the fMRI signal," Nature, Nature, vol. 412(6843), pages 150-157, July.
    2. Kendrick N. Kay & Thomas Naselaris & Ryan J. Prenger & Jack L. Gallant, 2008. "Identifying natural images from human brain activity," Nature, Nature, vol. 452(7185), pages 352-355, March.
    3. Russell Epstein & Nancy Kanwisher, 1998. "A cortical representation of the local visual environment," Nature, Nature, vol. 392(6676), pages 598-601, April.
    Full references (including those not matched with items on IDEAS)

    Citations

    Citations are extracted by the CitEc Project, subscribe to its RSS feed for this item.
    as


    Cited by:

    1. Hamed Nili & Cai Wingfield & Alexander Walther & Li Su & William Marslen-Wilson & Nikolaus Kriegeskorte, 2014. "A Toolbox for Representational Similarity Analysis," PLOS Computational Biology, Public Library of Science, vol. 10(4), pages 1-11, April.

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Zvi N. Roth & Kendrick Kay & Elisha P. Merriam, 2022. "Natural scene sampling reveals reliable coarse-scale orientation tuning in human V1," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    2. Marisa Nordt & Jesse Gomez & Vaidehi S. Natu & Alex A. Rezai & Dawn Finzi & Holly Kular & Kalanit Grill-Spector, 2023. "Longitudinal development of category representations in ventral temporal cortex predicts word and face recognition," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    3. Ying Wang & Xue Zhang & Chunhui Wang & Weifen Huang & Qian Xu & Dong Liu & Wen Zhou & Shanguang Chen & Yi Jiang, 2022. "Modulation of biological motion perception in humans by gravity," Nature Communications, Nature, vol. 13(1), pages 1-10, December.
    4. Joel Z Leibo & Qianli Liao & Fabio Anselmi & Tomaso Poggio, 2015. "The Invariance Hypothesis Implies Domain-Specific Regions in Visual Cortex," PLOS Computational Biology, Public Library of Science, vol. 11(10), pages 1-29, October.
    5. Isabella C. Wagner & Luise P. Graichen & Boryana Todorova & Andre Lüttig & David B. Omer & Matthias Stangl & Claus Lamm, 2023. "Entorhinal grid-like codes and time-locked network dynamics track others navigating through space," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    6. Umut Güçlü & Marcel A J van Gerven, 2014. "Unsupervised Feature Learning Improves Prediction of Human Brain Activity in Response to Natural Images," PLOS Computational Biology, Public Library of Science, vol. 10(8), pages 1-12, August.
    7. Guillermo A Cecchi & Lejian Huang & Javeria Ali Hashmi & Marwan Baliki & María V Centeno & Irina Rish & A Vania Apkarian, 2012. "Predictive Dynamics of Human Pain Perception," PLOS Computational Biology, Public Library of Science, vol. 8(10), pages 1-12, October.
    8. Doungmo Goufo, Emile F. & Mbehou, Mohamed & Kamga Pene, Morgan M., 2018. "A peculiar application of Atangana–Baleanu fractional derivative in neuroscience: Chaotic burst dynamics," Chaos, Solitons & Fractals, Elsevier, vol. 115(C), pages 170-176.
    9. Irene Neuner & Wolfram Kawohl & Jorge Arrubla & Tracy Warbrick & Konrad Hitz & Christine Wyss & Frank Boers & N Jon Shah, 2014. "Cortical Response Variation with Different Sound Pressure Levels: A Combined Event-Related Potentials and fMRI Study," PLOS ONE, Public Library of Science, vol. 9(10), pages 1-14, October.
    10. Hamed Nili & Cai Wingfield & Alexander Walther & Li Su & William Marslen-Wilson & Nikolaus Kriegeskorte, 2014. "A Toolbox for Representational Similarity Analysis," PLOS Computational Biology, Public Library of Science, vol. 10(4), pages 1-11, April.
    11. Hamed Nili & Alexander Walther & Arjen Alink & Nikolaus Kriegeskorte, 2020. "Inferring exemplar discriminability in brain representations," PLOS ONE, Public Library of Science, vol. 15(6), pages 1-28, June.
    12. Phoebe Koundouri & Barbara Hammer & Ulrike Kuhl & Alina Velias, 2022. "Behavioral and Neuroeconomics of Environmental Values," DEOS Working Papers 2227, Athens University of Economics and Business.
    13. Wan-Yu Shih & Hsiang-Yu Yu & Cheng-Chia Lee & Chien-Chen Chou & Chien Chen & Paul W. Glimcher & Shih-Wei Wu, 2023. "Electrophysiological population dynamics reveal context dependencies during decision making in human frontal cortex," Nature Communications, Nature, vol. 14(1), pages 1-24, December.
    14. Simon A Overduin & Philip Servos, 2008. "Symmetric Sensorimotor Somatotopy," PLOS ONE, Public Library of Science, vol. 3(1), pages 1-6, January.
    15. Amrita Pal & Jennifer A Ogren & Ravi S Aysola & Rajesh Kumar & Luke A Henderson & Ronald M Harper & Paul M Macey, 2021. "Insular functional organization during handgrip in females and males with obstructive sleep apnea," PLOS ONE, Public Library of Science, vol. 16(2), pages 1-22, February.
    16. Gavin Perry & Nathan W Taylor & Philippa C H Bothwell & Colette C Milbourn & Georgina Powell & Krish D Singh, 2020. "The gamma response to colour hue in humans: Evidence from MEG," PLOS ONE, Public Library of Science, vol. 15(12), pages 1-21, December.
    17. Jacob M. Paul & Martijn Ackooij & Tuomas C. Cate & Ben M. Harvey, 2022. "Numerosity tuning in human association cortices and local image contrast representations in early visual cortex," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    18. Olsen, Carmen & Gold, Anna, 2018. "Future research directions at the intersection between cognitive neuroscience research and auditors’ professional skepticism," Journal of Accounting Literature, Elsevier, vol. 41(C), pages 127-141.
    19. Ujwal Chaudhary & Bin Xia & Stefano Silvoni & Leonardo G Cohen & Niels Birbaumer, 2017. "Brain–Computer Interface–Based Communication in the Completely Locked-In State," PLOS Biology, Public Library of Science, vol. 15(1), pages 1-25, January.
    20. Chaogan Yan & Dongqiang Liu & Yong He & Qihong Zou & Chaozhe Zhu & Xinian Zuo & Xiangyu Long & Yufeng Zang, 2009. "Spontaneous Brain Activity in the Default Mode Network Is Sensitive to Different Resting-State Conditions with Limited Cognitive Load," PLOS ONE, Public Library of Science, vol. 4(5), pages 1-11, May.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:plo:pbio00:0060187. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: plosbiology (email available below). General contact details of provider: https://journals.plos.org/plosbiology/ .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.