Joint neuronal tuning for object form and position in the human lateral occipital complex

A long-standing heuristic in visual neuroscience holds that extrastriate visual cortex is parceled into a dorsal "where" pathway concerned with stimulus position and motion and a ventral "what" pathway concerned with stimulus form. Several recent studies using functional magnetic resonance imaging (fMRI), however, have shown that small changes in the position of a single object can produce reliable changes in activity patterns in object-selective lateral occipital complex (LOC). Although these data demonstrate that information about both object form and position is present at the region level in LOC, the extent to which they reflect joint neuronal tuning to these dimensions is unclear. To measure joint tuning for form and position, we used fMRI to record patterns of activity evoked in LOC and other visual areas while subjects viewed pairs of objects that varied in category content, overall position, and relative object position. Consistent with previous results, multivoxel activity patterns in LOC varied reliably with the category content and position of object pairs. Moreover, activity patterns in the lateral occipital (LO) subregion of LOC varied significantly with the relative positions of objects within pairs, even when absolute pair position was constant. This result provides strong evidence for the existence of neuronal populations in LO which are jointly tuned for both object form (i.e., category) and position.

[1]  Marcelo Gomes Mattar,et al.  de Bruijn cycles for neural decoding , 2011, NeuroImage.

[2]  Russell A. Epstein,et al.  Decoding the Representation of Multiple Simultaneous Objects in Human Occipitotemporal Cortex , 2009, Current Biology.

[3]  R. Vogels,et al.  Spatial sensitivity of macaque inferior temporal neurons , 2000, The Journal of comparative neurology.

[4]  Dwight J. Kravitz,et al.  How position dependent is visual object recognition? , 2008, Trends in Cognitive Sciences.

[5]  S. Edelman,et al.  Differential Processing of Objects under Various Viewing Conditions in the Human Lateral Occipital Complex , 1999, Neuron.

[6]  I. Biederman,et al.  Neural encoding of relative position. , 2011, Journal of experimental psychology. Human perception and performance.

[7]  P. Cavanagh,et al.  Retinotopy of the face aftereffect , 2008, Vision Research.

[8]  Dwight J. Kravitz,et al.  Real-World Scene Representations in High-Level Visual Cortex: It's the Spaces More Than the Places , 2011, The Journal of Neuroscience.

[9]  Hinze Hogendoorn,et al.  Spatial coding and invariance in object-selective cortex , 2011, Cortex.

[10]  J. Maunsell,et al.  Anterior inferotemporal neurons of monkeys engaged in object recognition can be highly sensitive to object retinal position. , 2003, Journal of neurophysiology.

[11]  G. Aguirre,et al.  Different spatial scales of shape similarity representation in lateral and ventral LOC. , 2009, Cerebral cortex.

[12]  Irving Biederman,et al.  Invariance of long-term visual priming to scale, reflection, translation, and hemisphere , 2001, Vision Research.

[13]  E. Rolls,et al.  Scene perception: inferior temporal cortex neurons encode the positions of different objects in the scene , 2005, The European journal of neuroscience.

[14]  K. Grill-Spector,et al.  Relating retinotopic and object-selective responses in human lateral occipital cortex. , 2008, Journal of neurophysiology.

[15]  I. Biederman,et al.  Evidence for Complete Translational and Reflectional Invariance in Visual Object Priming , 1991, Perception.

[16]  Matthias Niemeier,et al.  A contralateral preference in the lateral occipital area: sensory and attentional mechanisms. , 2004, Cerebral cortex.

[17]  David D. Cox,et al.  Functional magnetic resonance imaging (fMRI) “brain reading”: detecting and classifying distributed patterns of fMRI activity in human visual cortex , 2003, NeuroImage.

[18]  Thomas E. Nichols,et al.  Nonparametric permutation tests for functional neuroimaging: A primer with examples , 2002, Human brain mapping.

[19]  Nancy Kanwisher,et al.  Cerebral Cortex doi:10.1093/cercor/bhr357 Higher Level Visual Cortex Represents Retinotopic, Not Spatiotopic, Object Location , 2011 .

[20]  Z Kourtzi,et al.  Representation of Perceived Object Shape by the Human Lateral Occipital Complex , 2001, Science.

[21]  Li Fei-Fei,et al.  Neural mechanisms of rapid natural scene categorization in human visual cortex , 2009, Nature.

[22]  T. Carlson,et al.  Patterns of Activity in the Categorical Representations of Objects , 2003 .

[23]  Russell A. Epstein,et al.  Position selectivity in scene- and object-responsive occipitotemporal regions. , 2007, Journal of neurophysiology.

[24]  Leslie G. Ungerleider,et al.  Object vision and spatial vision: two cortical pathways , 1983, Trends in Neurosciences.

[25]  Nancy Kanwisher,et al.  The distribution of category and location information across object-selective regions in human visual cortex , 2008, Proceedings of the National Academy of Sciences.

[26]  Yi Chen,et al.  Encoding the identity and location of objects in human LOC , 2011, NeuroImage.

[27]  Russell A. Epstein,et al.  Distances between Real-World Locations Are Represented in the Human Hippocampus , 2011, The Journal of Neuroscience.

[28]  Radoslaw Martin Cichy,et al.  Probing principles of large‐scale object representation: Category preference and location encoding , 2013, Human brain mapping.

[29]  Ehud Zohary,et al.  Beyond retinotopic mapping: the spatial representation of objects in the human lateral occipital complex. , 2007, Cerebral cortex.

[30]  Russell A. Epstein,et al.  Constructing scenes from objects in human occipitotemporal cortex , 2011, Nature Neuroscience.

[31]  Dwight J. Kravitz,et al.  High-level visual object representations are constrained by position. , 2010, Cerebral cortex.

[32]  David Whitney,et al.  The Emergence of Perceived Position in the Visual System , 2011, Journal of Cognitive Neuroscience.

[33]  Russell A. Epstein,et al.  Differential parahippocampal and retrosplenial involvement in three types of visual scene recognition. , 2006, Cerebral cortex.