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

Highlights

• Leftward prism adaptation induces a long-lasting visuospatial shift.

• This shift in line bisection judgments takes time to develop fully.

• This shift lasts at least 35 min and fluctuates across time.

Abstract

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 40 min 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.

Introduction

Prism Adaptation (PA) is a classic technique for reversibly modifying sensorimotor correspondences and has been extensively investigated (Hay et al., 1971, Hein and Held, 1962, Held and Freedman, 1963, Held and Mikaelian, 1964, Helmholtz, 1867, Stratton, 1896; for review see Redding & Wallace, 2006). Wedge prisms produce a lateral shift of the visual field, and adaptation of hand pointing movements to displaced vision is now considered to be one of the most promising techniques for treating neglect symptoms (Luauté et al., 2006a, Milner and McIntosh, 2005, Newport and Schenk, 2012). Indeed, since the original demonstration of its efficacy in ameliorating performance on standard neuropsychological tests of neglect (copying a drawing, drawing from memory, reading) (Rossetti et al., 1998) PA has been shown to promote the resetting of the oculo-motor system (Serino, Angeli, Frassinetti, & Làdavas, 2006) and to improve performance on a range of tasks that tap into visuospatial cognition like line bisection (Pisella, Rode, Farnè, Boisson, & Rossetti, 2002), global/local processing (Bultitude, Rafal, & List, 2009), haptic exploration (McIntosh, Rossetti, & Milner, 2002), wheel-chair navigation (Jacquin-Courtois, Rode, Pisella, Boisson, & Rossetti, 2008), and visual imagery (Rode, Rossetti, & Boisson, 2001), possibly by acting mainly on the dorsal stream (Fortis et al., 2011, Striemer and Danckert, 2010b). PA also improves performance on non-visual tasks like tactile and auditory extinction (Jacquin-Courtois et al., 2010, Maravita et al., 2003).

In addition to its ability to reduce neglect symptoms in patient populations, a remarkable feature of PA is its ability to induce neglect-like behavior in healthy subjects. For example, PA changes behavior on visuospatial tasks like line bisection, greyscales, global/local processing, and haptic exploration (Berberovic and Mattingley, 2003, Bultitude and Woods, 2010, Colent et al., 2000, Girardi et al., 2004, Jackson and Newport, 2001, Loftus et al., 2009, Michel et al., 2003). It also alters spatial remapping (Bultitude, Van der Stigchel, & Nijboer, 2013) and the estimated duration of auditory stimuli (Magnani, Pavani, & Frassinetti, 2012). In this respect, PA is similar to some brain-modulation techniques, such as repetitive transcranial magnetic stimulation (rTMS) and transcranial direct current stimulation (tDCS), which can alleviate neglect symptoms in patients (Brighina et al., 2002, Koch et al., 2008, Oliveri et al., 2001, Sparing et al., 2009) and induce neglect-like behavior in healthy participants (Fierro et al., 2000, Giglia et al., 2011, Romei et al., 2011, Sparing et al., 2009).

It is important to note that the direction of the prismatic displacement is pivotal for improving neglect in patients or inducing neglect-like behavior in healthy subjects. Neglect symptoms in patients improve only after adaptation to rightward-deviating prisms (Luauté et al., 2012) and visuospatial performance in healthy subjects is shifted only after adaptation to leftward-deviating prisms (Berberovic and Mattingley, 2003, Colent et al., 2000, Michel et al., 2003, Nijboer et al., 2010). In addition to differing in terms of the direction of the prismatic displacement required to induce visuospatial adaptation effects, neglect patients and healthy subjects also differ with respect to the duration of these effects. For example, a single session of PA in neglect patients can significantly improve neglect symptoms for at least two hours (Rossetti et al., 1998) and in some patients for up to several days (Farnè et al., 2002, Pisella et al., 2002). Two-weeks of treatment can produce positive effects for one to six months (Frassinetti et al., 2002, Serino et al., 2007), and a single patient treated daily for three months still had improved detection of contralesional visual stimuli two years after the prism treatment (Nijboer, Nys, Van der Smagt, Van der Stigchel, & Dijkerman, 2011). In healthy subjects, perceptual changes are assumed to last only a few minutes, but this idea appears to come from the fact that almost all studies examined visuospatial effects only in the few minutes following adaptation, and not from data showing that these effects disappear at later times.

In this study we examined sensorimotor and visuospatial aftereffects in healthy participants multiple times after prism adaptation. Accuracy in open-loop pointing was used to measure the sensorimotor aftereffects and line bisection judgments measured the visuospatial aftereffect. Young participants typically make midline judgments to the left of the true center (Bowers and Heilman, 1980, Jewell and McCourt, 2000, Toba et al., 2011). This left bias is termed pseudoneglect, and there is a large body of evidence showing that adaptation to leftward-deviating prisms causes participants to shift their midline judgments to the right, thus reducing (Loftus et al., 2009, Nijboer et al., 2010), or cancelling (Colent et al., 2000, Berberovic and Mattingley, 2003, Michel et al., 2003) their pseudoneglect. Since we were particularly interested in the time course of visuospatial aftereffects produced by PA we designed a pre/multiple-posts experiment in which we assessed pointing accuracy and midline judgments every 5 min for 40 min after a single session of PA.