Sensitive Period for a Multimodal Response in Human Visual Motion Area MT/MST

The middle temporal complex (MT/MST) is a brain region specialized for the perception of motion in the visual modality. However, this specialization is modified by visual experience: after long-standing blindness, MT/MST responds to sound. Recent evidence also suggests that the auditory response of MT/MST is selective for motion. The developmental time course of this plasticity is not known. To test for a sensitive period in MT/MST development, we used fMRI to compare MT/MST function in congenitally blind, late-blind, and sighted adults. MT/MST responded to sound in congenitally blind adults, but not in late-blind or sighted adults, and not in an individual who lost his vision between ages of 2 and 3 years. All blind adults had reduced functional connectivity between MT/MST and other visual regions. Functional connectivity was increased between MT/MST and lateral prefrontal areas in congenitally blind relative to sighted and late-blind adults. These data suggest that early blindness affects the function of feedback projections from prefrontal cortex to MT/MST. We conclude that there is a sensitive period for visual specialization in MT/MST. During typical development, early visual experience either maintains or creates a vision-dominated response. Once established, this response profile is not altered by long-standing blindness.

[1]  D. Maurer,et al.  Better perception of global motion after monocular than after binocular deprivation , 2002, Vision Research.

[2]  G H Recanzone,et al.  Effects of attention on MT and MST neuronal activity during pursuit initiation. , 2000, Journal of neurophysiology.

[3]  Gianluca Campana,et al.  Visual area V5/MT remembers "what" but not "where". , 2004, Cerebral cortex.

[4]  H. Burton Visual Cortex Activity in Early and Late Blind People , 2003, The Journal of Neuroscience.

[5]  T. L. Lewis,et al.  Greater losses in sensitivity to second-order local motion than to first-order local motion after early visual deprivation in humans , 2005, Vision Research.

[6]  Thomas T. Liu,et al.  A component based noise correction method (CompCor) for BOLD and perfusion based fMRI , 2007, NeuroImage.

[7]  J. Haxby,et al.  The effect of visual experience on the development of functional architecture in hMT+. , 2007, Cerebral cortex.

[8]  J. Atkinson,et al.  Reorganization of Global Form and Motion Processing during Human Visual Development , 2010, Current Biology.

[9]  N. Kanwisher,et al.  Activation in Human MT/MST by Static Images with Implied Motion , 2000, Journal of Cognitive Neuroscience.

[10]  Michela Gamberini,et al.  Cytoarchitectonic subdivisions of the dorsolateral frontal cortex of the marmoset monkey (Callithrix jacchus), and their projections to dorsal visual areas , 2006, The Journal of comparative neurology.

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

[12]  B. Biswal,et al.  Functional connectivity in the motor cortex of resting human brain using echo‐planar mri , 1995, Magnetic resonance in medicine.

[13]  C. Büchel,et al.  Modulation of connectivity in visual pathways by attention: cortical interactions evaluated with structural equation modelling and fMRI. , 1997, Cerebral cortex.

[14]  Manabu Honda,et al.  Critical Period for Cross-Modal Plasticity in Blind Humans: A Functional MRI Study , 2002, NeuroImage.

[15]  Norihiro Sadato,et al.  An investigation of cross-modal plasticity of effective connectivity in the blind by dynamic causal modeling of functional MRI data , 2009, Neuroscience Research.

[16]  Franco Lepore,et al.  Differential occipital responses in early- and late-blind individuals during a sound-source discrimination task , 2008, NeuroImage.

[17]  Joost X. Maier,et al.  Natural, Metaphoric, and Linguistic Auditory Direction Signals Have Distinct Influences on Visual Motion Processing , 2009, The Journal of Neuroscience.

[18]  Alexander G. Huth,et al.  Visual Motion Area MT+/V5 Responds to Auditory Motion in Human Sight-Recovery Subjects , 2008, The Journal of Neuroscience.

[19]  Abraham Z. Snyder,et al.  A method for using blocked and event-related fMRI data to study “resting state” functional connectivity , 2007, NeuroImage.

[20]  E. DeYoe,et al.  A comparison of visual and auditory motion processing in human cerebral cortex. , 2000, Cerebral cortex.

[21]  E. Miller,et al.  An integrative theory of prefrontal cortex function. , 2001, Annual review of neuroscience.

[22]  Karl J. Friston,et al.  Early visual deprivation induces structural plasticity in gray and white matter , 2005, Current Biology.

[23]  Thomas E. Nichols,et al.  Combining voxel intensity and cluster extent with permutation test framework , 2004, NeuroImage.

[24]  Karl J. Friston,et al.  How Many Subjects Constitute a Study? , 1999, NeuroImage.

[25]  S. Thompson-Schill,et al.  The frontal lobes and the regulation of mental activity , 2005, Current Opinion in Neurobiology.

[26]  A. Caramazza,et al.  Concepts Are More than Percepts: The Case of Action Verbs , 2008, The Journal of Neuroscience.

[27]  M. Fox,et al.  Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging , 2007, Nature Reviews Neuroscience.

[28]  R. Andersen,et al.  Functional analysis of human MT and related visual cortical areas using magnetic resonance imaging , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[29]  Alan C. Evans,et al.  A new anatomical landmark for reliable identification of human area V5/MT: a quantitative analysis of sulcal patterning. , 2000, Cerebral cortex.

[30]  Sophie M. Wuerger,et al.  Low-level integration of auditory and visual motion signals requires spatial co-localisation , 2005, Experimental Brain Research.

[31]  D. Maurer,et al.  Multiple sensitive periods in human visual development: evidence from visually deprived children. , 2005, Developmental psychobiology.

[32]  Michael Erb,et al.  Object-selective responses in the human motion area MT/MST , 2002, Nature Neuroscience.

[33]  Current Biology , 2012, Current Biology.

[34]  Colline Poirier,et al.  Auditory motion perception activates visual motion areas in early blind subjects , 2006, NeuroImage.

[35]  T. Egner,et al.  Cognitive control mechanisms resolve conflict through cortical amplification of task-relevant information , 2005, Nature Neuroscience.

[36]  M. Raichle,et al.  Adaptive changes in early and late blind: a FMRI study of verb generation to heard nouns. , 2002, Journal of neurophysiology.

[37]  Richard S. J. Frackowiak,et al.  Area V5 of the human brain: evidence from a combined study using positron emission tomography and magnetic resonance imaging. , 1993, Cerebral cortex.

[38]  Archana Venkataraman,et al.  Intrinsic functional connectivity as a tool for human connectomics: theory, properties, and optimization. , 2010, Journal of neurophysiology.

[39]  Karen R Dobkins,et al.  Does visual modularity increase over the course of development? , 2009, Optometry and vision science : official publication of the American Academy of Optometry.

[40]  Vince D. Calhoun,et al.  Measuring brain connectivity: Diffusion tensor imaging validates resting state temporal correlations , 2008, NeuroImage.

[41]  S. Zeki,et al.  The cerebral activity related to the visual perception of forward motion in depth. , 1994, Brain : a journal of neurology.

[42]  Justin L. Vincent,et al.  Distinct brain networks for adaptive and stable task control in humans , 2007, Proceedings of the National Academy of Sciences.

[43]  S. Zeki,et al.  Response properties and receptive fields of cells in an anatomically defined region of the superior temporal sulcus in the monkey. , 1971, Brain research.

[44]  T. Pasternak,et al.  Directional Signals in the Prefrontal Cortex and in Area MT during a Working Memory for Visual Motion Task , 2006, The Journal of Neuroscience.

[45]  M. Greicius,et al.  Resting-state functional connectivity reflects structural connectivity in the default mode network. , 2009, Cerebral cortex.

[46]  S. Wuerger,et al.  Cross-modal integration of auditory and visual motion signals , 2001, Neuroreport.

[47]  N. Mai,et al.  Selective disturbance of movement vision after bilateral brain damage. , 1983, Brain : a journal of neurology.

[48]  Marcello G P Rosa,et al.  Hierarchical development of the primate visual cortex, as revealed by neurofilament immunoreactivity: early maturation of the middle temporal area (MT). , 2006, Cerebral cortex.

[49]  Chunshui Yu,et al.  Whole brain functional connectivity in the early blind. , 2007, Brain : a journal of neurology.

[50]  Pavel Zahorik,et al.  Decoding the direction of auditory motion in blind humans , 2011, NeuroImage.

[51]  S. Rombouts,et al.  Consistent resting-state networks across healthy subjects , 2006, Proceedings of the National Academy of Sciences.