Prism adaptation in the healthy brain: The shift in line bisection judgments is long lasting and fluctuates

Rightward prism adaptation has been shown to ameliorate visuospatial biases in right brain-damaged patients with neglect, and a single session of prism adaptation can lead to improvements that last up to several hours. Leftward prism adaptation in neurologically healthy individuals induces neglect-like biases in visuospatial tasks. The duration of these effects in healthy individuals, typically assumed to be ephemeral, has never been investigated. Here we assessed the time-course of the adaptation-induced modifications in a classical perceptual line bisection task that was repeatedly administered for approximately 40min after a single session of adaptation to either a leftward or rightward prismatic deviation. Consistent with previous reports, only adaptation to leftward-deviating prisms induced a visuospatial shift on perceptual line bisection judgments. The typical pattern of pseudoneglect was counteracted by a rightward shift in midline judgments, which became significant between 5 and 10 min after adaptation, fluctuated between being significant or not several times in the 40 min following adaptation, and was present as late as 35 min. In contrast, the sensorimotor aftereffect was present immediately after adaptation to both rightward and leftward deviating prisms, decayed initially then remained stable until 40 min. These results demonstrate that both the sensorimotor and visuospatial effects last for at least 35 min, but that the visuospatial shift needs time to fully develop and fluctuates. By showing that the effects of prism adaptation in the undamaged brain are not ephemeral, these findings reveal the presence of another, so-far neglected dimension in the domain of the cognitive effects induced by prism adaptation, namely time. The prolonged duration of the induced visuospatial shift, previously considered to be a feature of prism adaptation unique to brain-damaged subjects, also applies to the normal brain.

[1]  M. Perenin,et al.  Prism adaptation to a rightward optical deviation rehabilitates left hemispatial neglect , 1998, Nature.

[2]  Juan Fernández-Ruiz,et al.  Decay of prism aftereffects under passive and active conditions. , 2004, Brain research. Cognitive brain research.

[3]  H L Pick,et al.  Spatial parameters of eye-hand adaptation to optical distortion. , 1971, Journal of experimental psychology.

[4]  Y. Rossetti,et al.  Sensorimotor effects on central space representation: prism adaptation influences haptic and visual representations in normal subjects , 2004, Neuropsychologia.

[5]  Y. Rossetti,et al.  Functional anatomy of the therapeutic effects of prism adaptation on left neglect , 2006, Neurology.

[6]  Yves Rossetti,et al.  Enhancing Visuomotor Adaptation by Reducing Error Signals: Single-step (Aware) versus Multiple-step (Unaware) Exposure to Wedge Prisms , 2007, Journal of Cognitive Neuroscience.

[7]  R. Held,et al.  PLASTICITY IN HUMAN SENSORIMOTOR CONTROL. , 1963, Science.

[8]  Y. Rossetti,et al.  Left-Deviating Prism Adaptation in Left Neglect Patient: Reflexions on a Negative Result , 2012, Neural plasticity.

[9]  Y. Rossetti,et al.  Effect of prism adaptation on left dichotic listening deficit in neglect patients: glasses to hear better? , 2010, Brain : a journal of neurology.

[10]  Yves Rossetti,et al.  Dissociated long lasting improvements of straight-ahead pointing and line bisection tasks in two hemineglect patients , 2002, Neuropsychologia.

[11]  Patrick Cavanagh,et al.  Attention biases the perceived midpoint of horizontal lines , 2011, Neuropsychologia.

[12]  E. Bisiach,et al.  rTMS of the unaffected hemisphere transiently reduces contralesional visuospatial hemineglect , 2001, Neurology.

[13]  S. Stigchel,et al.  Prism adaptation alters spatial remapping in healthy individuals: Evidence from double-step saccades , 2013, Cortex.

[14]  Y. Rossetti,et al.  Two waves of a long-lasting aftereffect of prism adaptation measured over 7 days , 2006, Experimental Brain Research.

[15]  R. Held,et al.  Motor-Sensory Feedback versus Need in Adaptation to Rearrangement , 1964, Perceptual and motor skills.

[16]  Filippo Brighina,et al.  Contralateral neglect induced by right posterior parietal rTMS in healthy subjects , 2000, Neuroreport.

[17]  G. Stratton Some preliminary experiments on vision without inversion of the retinal image. , 1896 .

[18]  C. Caltagirone,et al.  Theta-burst stimulation of the left hemisphere accelerates recovery of hemispatial neglect , 2012, Neurology.

[19]  A. Milner,et al.  Prism Adaptation Improves Chronic Visual and Haptic Neglect: A Single Case Study , 2002, Cortex.

[20]  K. Goedert,et al.  Prism adaptation differently affects motor-intentional and perceptual-attentional biases in healthy individuals , 2011, Neuropsychologia.

[21]  Y. Rossetti,et al.  Ameliorating neglect with prism adaptation: visuo-manual and visuo-verbal measures , 2002, Neuropsychologia.

[22]  Filippo Brighina,et al.  Perceptual and response bias in visuospatial neglect due to frontal and parietal repetitive transcranial magnetic stimulation in normal subjects , 2002, Neuroreport.

[23]  J. Bultitude,et al.  Adaptation to leftward-shifting prisms reduces the global processing bias of healthy individuals , 2010, Neuropsychologia.

[24]  Gregor Thut,et al.  Rhythmic TMS over Parietal Cortex Links Distinct Brain Frequencies to Global versus Local Visual Processing , 2011, Current Biology.

[25]  Y. Rossetti,et al.  Prism adaptation in the rehabilitation of patients with visuo-spatial cognitive disorders , 2006, Current opinion in neurology.

[26]  J. Lackner,et al.  Adaptation to Displaced Vision: Evidence for Prolonged After-Effects , 1977, The Quarterly journal of experimental psychology.

[27]  J. Rothwell,et al.  Hyperexcitability of parietal-motor functional connections in the intact left-hemisphere of patients with neglect. , 2008, Brain : a journal of neurology.

[28]  M. Saoud,et al.  Finding centre: Ocular and fMRI investigations of bisection and landmark task performance , 2012, Brain Research.

[29]  K. Zilles,et al.  Line bisection judgments implicate right parietal cortex and cerebellum as assessed by fMRI , 2000, Neurology.

[30]  F. Meneghello,et al.  Long-lasting amelioration of visuospatial neglect by prism adaptation. , 2002, Brain : a journal of neurology.

[31]  C. Caltagirone,et al.  Asymmetry of Parietal Interhemispheric Connections in Humans , 2011, The Journal of Neuroscience.

[32]  Stuart T. Klapp,et al.  Long-lasting aftereffect of brief prism exposure , 1974 .

[33]  Roger Newport,et al.  Prisms and neglect: What have we learned? , 2012, Neuropsychologia.

[34]  Y. Rossetti,et al.  Wheel-chair driving improvement following visuo-manual prism adaptation , 2008, Cortex.

[35]  Massimiliano Oliveri,et al.  Brain stimulation procedures for treatment of contralesional spatial neglect. , 2011, Restorative neurology and neuroscience.

[36]  Jeannine Herron,et al.  Differential right hemisphere engagement in visuospatial tasks , 1980, Neuropsychologia.

[37]  M. Nicholls,et al.  Prism adaptation overcomes pseudoneglect for the greyscales task , 2009, Cortex.

[38]  E. Làdavas,et al.  Neglect treatment by prism adaptation: What recovers and for how long , 2007, Neuropsychological rehabilitation.

[39]  James Danckert,et al.  Dissociating perceptual and motor effects of prism adaptation in neglect , 2010, Neuroreport.

[40]  Shigeru Kitazawa,et al.  Long-lasting aftereffects of prism adaptation in the monkey , 2001, Experimental Brain Research.

[41]  K. Heilman,et al.  Pseudoneglect: Effects of hemispace on a tactile line bisection task , 1980, Neuropsychologia.

[42]  R B Welch,et al.  Variables affecting the intermanual transfer and decay of prism adaptation. , 1974, Journal of experimental psychology.

[43]  Y. Rossetti,et al.  Prism adaptation improves representational neglect , 2001, Neuropsychologia.

[44]  J. Danckert,et al.  Through a prism darkly: re-evaluating prisms and neglect , 2010, Trends in Cognitive Sciences.

[45]  Y. Rossetti,et al.  Simulating unilateral neglect in normals using prism adaptation: implications for theory , 2003, Neuropsychologia.

[46]  P. Astikainen,et al.  Cortical and subcortical visual event‐related potentials to oddball stimuli in rabbits , 2000, Neuroreport.

[47]  Stefan Van der Stigchel,et al.  Prism adaptation influences perception but not attention: evidence from antisaccades , 2010, Neuroreport.

[48]  Jason B Mattingley,et al.  Effects of prismatic adaptation on judgements of spatial extent in peripersonal and extrapersonal space , 2003, Neuropsychologia.

[49]  B. Fierro,et al.  Neglect-like effects induced by tDCS modulation of posterior parietal cortices in healthy subjects , 2011, Brain Stimulation.

[50]  E. Làdavas,et al.  Mechanisms underlying neglect recovery after prism adaptation , 2006, Neuropsychologia.

[51]  Y. Rossetti,et al.  Cognitive bias induced by visuo‐motor adaptation to prisms: a simulation of unilateral neglect in normal individuals? , 2000, Neuroreport.

[52]  P. Vuilleumier,et al.  Unilateral spatial neglect recovery after sequential strokes , 1996, Neurology.

[53]  Roger Newport,et al.  Prism adaptation produces neglect-like patterns of hand path curvature in healthy adults , 2001, Neuropsychologia.

[54]  Gordon M. Redding,et al.  Prism adaptation and unilateral neglect: Review and analysis , 2006, Neuropsychologia.

[55]  Robert D McIntosh,et al.  The neurological basis of visual neglect , 2005, Current opinion in neurology.

[56]  M. Corbetta,et al.  Neural basis and recovery of spatial attention deficits in spatial neglect , 2005, Nature Neuroscience.

[57]  Patrik Vuilleumier,et al.  Prism adaptation enhances activity of intact fronto-parietal areas in both hemispheres in neglect patients , 2013, Cortex.

[58]  G. Fink,et al.  Bidirectional alterations of interhemispheric parietal balance by non-invasive cortical stimulation. , 2009, Brain : a journal of neurology.

[59]  R. Held,et al.  A Neural Model for Labile Sensorimotor Coordinations , 1962 .

[60]  H. C. Dijkerman,et al.  Repetitive long-term prism adaptation permanently improves the detection of contralesional visual stimuli in a patient with chronic neglect , 2011, Cortex.

[61]  H. Helmholtz Handbuch der physiologischen Optik , 2015 .

[62]  A. Kral,et al.  Erratum to “Development of Brainstem-Evoked Responses in Congenital Auditory Deprivation” , 2012, Neural Plasticity.

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

[64]  Prism adaptation reverses the local processing bias in patients with right temporo-parietal junction lesions , 2010 .

[65]  F. Pavani,et al.  Changing auditory time with prismatic goggles , 2012, Cognition.

[66]  M. McCourt,et al.  Pseudoneglect: a review and meta-analysis of performance factors in line bisection tasks , 2000, Neuropsychologia.

[67]  Edward Taub,et al.  Prism Adaptation: Control of Intermanual Transfer by Distribution of Practice , 1973, Science.

[68]  Peter Halligan,et al.  Prism adaptation first among equals in alleviating left neglect: a review. , 2006, Restorative neurology and neuroscience.