Short-term plasticity of visuo-haptic object recognition

Functional magnetic resonance imaging (fMRI) studies have provided ample evidence for the involvement of the lateral occipital cortex (LO), fusiform gyrus (FG), and intraparietal sulcus (IPS) in visuo-haptic object integration. Here we applied 30 min of sham (non-effective) or real offline 1 Hz repetitive transcranial magnetic stimulation (rTMS) to perturb neural processing in left LO immediately before subjects performed a visuo-haptic delayed-match-to-sample task during fMRI. In this task, subjects had to match sample (S1) and target (S2) objects presented sequentially within or across vision and/or haptics in both directions (visual-haptic or haptic-visual) and decide whether or not S1 and S2 were the same objects. Real rTMS transiently decreased activity at the site of stimulation and remote regions such as the right LO and bilateral FG during haptic S1 processing. Without affecting behavior, the same stimulation gave rise to relative increases in activation during S2 processing in the right LO, left FG, bilateral IPS, and other regions previously associated with object recognition. Critically, the modality of S2 determined which regions were recruited after rTMS. Relative to sham rTMS, real rTMS induced increased activations during crossmodal congruent matching in the left FG for haptic S2 and the temporal pole for visual S2. In addition, we found stronger activations for incongruent than congruent matching in the right anterior parahippocampus and middle frontal gyrus for crossmodal matching of haptic S2 and in the left FG and bilateral IPS for unimodal matching of visual S2, only after real but not sham rTMS. The results imply that a focal perturbation of the left LO triggers modality-specific interactions between the stimulated left LO and other key regions of object processing possibly to maintain unimpaired object recognition. This suggests that visual and haptic processing engage partially distinct brain networks during visuo-haptic object matching.

[1]  Glyn W. Humphreys,et al.  Haptic Shape Processing in Visual Cortex , 2014, Journal of Cognitive Neuroscience.

[2]  Mareike M. Menz,et al.  Multisensory interactions between auditory and haptic object recognition. , 2013, Cerebral cortex.

[3]  Hartwig R. Siebner,et al.  Vision holds a greater share in visuo-haptic object recognition than touch , 2013, NeuroImage.

[4]  Nadia Bolognini,et al.  Cross-modal Processing in the Occipito-temporal Cortex: A TMS Study of the Müller-Lyer Illusion , 2011, Journal of Cognitive Neuroscience.

[5]  Hartwig R. Siebner,et al.  The left fusiform gyrus hosts trisensory representations of manipulable objects , 2011, NeuroImage.

[6]  Jochen Kaiser,et al.  Audiovisual Functional Magnetic Resonance Imaging Adaptation Reveals Multisensory Integration Effects in Object-Related Sensory Cortices , 2010, The Journal of Neuroscience.

[7]  Rainer Goebel,et al.  fMR-adaptation indicates selectivity to audiovisual content congruency in distributed clusters in human superior temporal cortex , 2010, BMC Neuroscience.

[8]  J. Rothwell,et al.  How does transcranial magnetic stimulation modify neuronal activity in the brain? Implications for studies of cognition , 2009, Cortex.

[9]  Amir Amedi,et al.  Multisensory visual–tactile object related network in humans: insights gained using a novel crossmodal adaptation approach , 2009, Experimental Brain Research.

[10]  Johannes Rüter,et al.  The Anatomy of Object Recognition—Visual Form Agnosia Caused by Medial Occipitotemporal Stroke , 2009, The Journal of Neuroscience.

[11]  P. Rossini,et al.  Consensus paper: Combining transcranial stimulation with neuroimaging , 2009, Brain Stimulation.

[12]  J. Devlin,et al.  Triple Dissociation of Faces, Bodies, and Objects in Extrastriate Cortex , 2009, Current Biology.

[13]  Jan Gläscher,et al.  Visualization of Group Inference Data in Functional Neuroimaging , 2009, Neuroinformatics.

[14]  Randall Stilla,et al.  Selective visuo‐haptic processing of shape and texture , 2008, Human brain mapping.

[15]  Michael S. Beauchamp,et al.  Touch, sound and vision in human superior temporal sulcus , 2008, NeuroImage.

[16]  B. Mesquita,et al.  Adjustment to Chronic Diseases and Terminal Illness Health Psychology : Psychological Adjustment to Chronic Disease , 2006 .

[17]  Michael J. Martinez,et al.  Bias between MNI and Talairach coordinates analyzed using the ICBM‐152 brain template , 2007, Human brain mapping.

[18]  William M. Stern,et al.  Shape conveyed by visual-to-auditory sensory substitution activates the lateral occipital complex , 2007, Nature Neuroscience.

[19]  N. Kanwisher,et al.  Only some spatial patterns of fMRI response are read out in task performance , 2007, Nature Neuroscience.

[20]  M. Rushworth,et al.  Functionally Specific Reorganization in Human Premotor Cortex , 2007, Neuron.

[21]  M. Ernst,et al.  Optimal integration of shape information from vision and touch , 2007, Experimental Brain Research.

[22]  Karl J. Friston,et al.  Acute Changes in Frontoparietal Activity after Repetitive Transcranial Magnetic Stimulation over the Dorsolateral Prefrontal Cortex in a Cued Reaction Time Task , 2006, The Journal of Neuroscience.

[23]  T. Rogers,et al.  Anterior temporal cortex and semantic memory: Reconciling findings from neuropsychology and functional imaging , 2006, Cognitive, affective & behavioral neuroscience.

[24]  Alan Cowey,et al.  TMS can reveal contrasting functions of the dorsal and ventral visual processing streams , 2006, Experimental Brain Research.

[25]  Tracy R. Henderson,et al.  Simple metric for scaling motor threshold based on scalp-cortex distance: application to studies using transcranial magnetic stimulation. , 2005, Journal of neurophysiology.

[26]  Simon B. Eickhoff,et al.  A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data , 2005, NeuroImage.

[27]  Paul J. Laurienti,et al.  Semantic congruence is a critical factor in multisensory behavioral performance , 2004, Experimental Brain Research.

[28]  B. Argall,et al.  Integration of Auditory and Visual Information about Objects in Superior Temporal Sulcus , 2004, Neuron.

[29]  Richard S. J. Frackowiak,et al.  Patients with focal arm dystonia have increased sensitivity to slow-frequency repetitive TMS of the dorsal premotor cortex. , 2003, Brain : a journal of neurology.

[30]  Karl J. Friston,et al.  Acute Remapping within the Motor System Induced by Low-Frequency Repetitive Transcranial Magnetic Stimulation , 2003, The Journal of Neuroscience.

[31]  Norihiro Sadato,et al.  Tactile-visual cross-modal shape matching: a functional MRI study. , 2003, Brain research. Cognitive brain research.

[32]  Ravi S. Menon,et al.  Haptic study of three-dimensional objects activates extrastriate visual areas , 2002, Neuropsychologia.

[33]  T. Hendler,et al.  Convergence of visual and tactile shape processing in the human lateral occipital complex. , 2002, Cerebral cortex.

[34]  K. Zilles,et al.  Crossmodal Processing of Object Features in Human Anterior Intraparietal Cortex An fMRI Study Implies Equivalencies between Humans and Monkeys , 2002, Neuron.

[35]  R. Malach,et al.  The topography of high-order human object areas , 2002, Trends in Cognitive Sciences.

[36]  J. Haxby,et al.  Parallel Visual Motion Processing Streams for Manipulable Objects and Human Movements , 2002, Neuron.

[37]  M. Ernst,et al.  Humans integrate visual and haptic information in a statistically optimal fashion , 2002, Nature.

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

[39]  J. Rothwell,et al.  Decreased corticospinal excitability after subthreshold 1 Hz rTMS over lateral premotor cortex , 2001, NeuroImage.

[40]  Alex Martin,et al.  Semantic memory and the brain: structure and processes , 2001, Current Opinion in Neurobiology.

[41]  T. Hendler,et al.  Visuo-haptic object-related activation in the ventral visual pathway , 2001, Nature Neuroscience.

[42]  M. Bar,et al.  Cortical Mechanisms Specific to Explicit Visual Object Recognition , 2001, Neuron.

[43]  K. Grill-Spector,et al.  The dynamics of object-selective activation correlate with recognition performance in humans , 2000, Nature Neuroscience.

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

[45]  A. Damasio,et al.  A neural basis for lexical retrieval , 1996, Nature.

[46]  Richard D. Hichwa,et al.  A neural basis for lexical retrieval , 1996, Nature.

[47]  R. Malach,et al.  Object-related activity revealed by functional magnetic resonance imaging in human occipital cortex. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[48]  L. Jakobson,et al.  A neurological dissociation between perceiving objects and grasping them , 1991, Nature.

[49]  M. Torrens Co-Planar Stereotaxic Atlas of the Human Brain—3-Dimensional Proportional System: An Approach to Cerebral Imaging, J. Talairach, P. Tournoux. Georg Thieme Verlag, New York (1988), 122 pp., 130 figs. DM 268 , 1990 .

[50]  A. Damasio Time-locked multiregional retroactivation: A systems-level proposal for the neural substrates of recall and recognition , 1989, Cognition.

[51]  Kenneth M. Heilman,et al.  Multimodal agnosia after unilateral left hemisphere lesion , 1986, Neurology.

[52]  R. C. Oldfield The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

[53]  M. Annett A classification of hand preference by association analysis. , 1970, British journal of psychology.

[54]  Á. Pascual-Leone,et al.  Transcranial Magnetic Stimulation , 2014, Neuromethods.

[55]  K Sathian,et al.  Multisensory object representation: insights from studies of vision and touch. , 2011, Progress in brain research.

[56]  T. Stanford,et al.  Multisensory integration: current issues from the perspective of the single neuron , 2008, Nature Reviews Neuroscience.

[57]  J. Rothwell,et al.  Transcranial magnetic stimulation: new insights into representational cortical plasticity , 2002, Experimental Brain Research.

[58]  J. Teijeiro-Amador,et al.  REV NEUROL , 2001 .

[59]  P. Courtheoux,et al.  [Visual and tactile agnosia]. , 1984, Revue neurologique.