Carine Michel1,2*- 1Unité de Formation et de Recherche en Sciences et Techniques des Activités Physiques et Sportives, Campus Universitaire, Université de Bourgogne, Dijon, France
- 2INSERM, U 1093, Cognition, Action et Plasticité Sensorimotrice, Dijon, France
Sensorimotor plasticity allows us to maintain an efficient motor behavior in reaction to environmental changes. One of the classical models for the study of sensorimotor plasticity is prism adaptation. It consists of pointing to visual targets while wearing prismatic lenses that shift the visual field laterally. The conditions of the development of the plasticity and the sensorimotor after-effects have been extensively studied for more than a century. However, the interest taken in this phenomenon was considerably increased since the demonstration of neglect rehabilitation following prism adaptation by Rossetti et al. (1998). Mirror effects, i.e., simulation of neglect in healthy individuals, were observed for the first time by Colent et al. (2000). The present review focuses on the expansion of prism adaptation to cognitive functions in healthy individuals during the last 15 years. Cognitive after-effects have been shown in numerous tasks even in those that are not intrinsically spatial in nature. Altogether, these results suggest the existence of a strong link between low-level sensorimotor plasticity and high-level cognitive functions and raise important questions about the mechanisms involved in producing unexpected cognitive effects following prism adaptation. Implications for the functional mechanisms and neuroanatomical network of prism adaptation are discussed to explain how sensorimotor plasticity may affect cognitive processes.
Introduction
Sensorimotor plasticity allows producing an appropriate motor response in reaction to environmental changes or bodily evolution during the life. Prism adaptation is one of the oldest paradigms to study sensorimotor plasticity. It consists of pointing to visual targets while wearing prismatic lenses that shift the visual field laterally. The pointing errors made in the direction of the optical shift are gradually corrected. After prism removal, the pointing movements are shifted in the direction opposite to the optical deviation. The entire process can be explained by proprioceptive, visual, and motor control changes (e.g., Kornheiser, 1976). Prism adaptation has been described for more than one century (e.g., Stratton, 1896) but the interest taken in this procedure was considerably increased since the publication of the article of Rossetti et al. (1998) showing the therapeutic impact of prism adaptation in neglect rehabilitation (Newport and Schenk, 2012). Neglect is described as a failure to report, respond, or orient to novel or meaningful stimuli presented to the side opposite to a brain lesion usually in the right hemisphere (e.g., Heilman et al., 1993). In their comprehensive review, Jacquin-Courtois et al. (2013) set out the therapeutic interest of prism adaptation on a broad range of clinical and experimental measures beyond the framework of sensorimotor coordination. The present revue focuses on the cognitive after-effects of prism adaptation in healthy individuals and presents this procedure as a robust tool for simulating neglect in normals. In the light of the recent results, it offers potential insights into the understanding of the expansion of low-level sensorimotor processes to cognitive functions.
Cognitive After-Effects of Prism Adaptation in Space Representation
The first demonstration of prism-induced cognitive after-effects in space representation (mental image of the space mapped across the brain) in healthy individuals was shown Colent et al. (2000). Line bisection task is an invaluable tool to assess space representation. In the manual version, subjects place a mark at the center of a horizontal line. In the perceptual judgment version (landmark test), they are requested to judge whether a line has been transected to the left or the right of its true center. Performance in healthy subjects is characterized by a leftward pseudoneglect bias due to a mental over-representation of the left part of space and an under-representation of the right part of space (e.g., McCourt and Jewell, 1999). Neglect patients show a rightward bias because they exhibit a mental under-representation of the left part of space and an over-representation of the right part of space (e.g., Halligan, 1995). When adaptation was developed by visuo-manual pointings with the right dominant hand during prism exposure (20 min under 15° leftward or rightward deviation), only adaptation to a leftward optical deviation produced representational after-effects. They appeared to be a faithful qualitative simulation of neglect, i.e., a rightward bias in perceptual line bisection (Colent et al., 2000). Complementary studies confirmed the effects of adaptation on both manual and perceptual bisection tasks (Michel et al., 2003a; Nijboer et al., 2010; Striemer and Danckert, 2010; Fortis et al., 2011; Michel and Cruz, 2015) and showed that they lasted for at least half an hour (Schintu et al., 2014). The occurrence of cognitive after-effects in healthy individuals seems to depend on the baseline expression of pseudoneglect. A greater leftward magnitude at baseline is associated with greater rightward after-effects (Goedert et al., 2010; Herlihey et al., 2012). Therefore, individuals with leftward bias due to right hemisphere dominance (e.g., Fink et al., 2001) are particularly sensitive to adaptation to leftward optical deviation that may act on right hemisphere functioning (see paragraph 5). This could also be the reason why experimental conditions involving the right hemisphere, as left-sided location of the line, favor the occurrence of cognitive after-effects (Michel et al., 2003a) and why no after-effect was observed in manual line bisection in the absence of baseline pseudoneglect (Colent et al., 2000).
Cross-modal after-effects of prism adaptation are observed on haptic tasks where participants are required to locate the center of a haptically explored circle or a visually perceived circle. Prism adaptation induced a rightward shift of performance similar to the bias shown in neglect patients (McIntosh et al., 2002; Girardi et al., 2004). Cognitive after-effects also extend to extrapersonal representation, i.e., beyond the immediate region (arm reach) within which visuomotor adaptation takes place. They were shown in the landmark task (Berberovic and Mattingley, 2003) and in goal-oriented locomotion (Michel et al., 2008). They are similar to neglect-like locomotor bias (Robertson et al., 1994; Berti et al., 2002). Cognitive after-effects even occur in mental scales. The mental number line is thought to have a left-to-right organization whereby low and high numbers are represented along a spatial continuum from left to right (Dehaene et al., 1993). As a result, when judging the distance between two numbers, without using arithmetic, normal subjects misbisect the mental distance toward the smaller number (i.e., to the left) (Longo and Lourenco, 2007; Loftus et al., 2009a). Adaptation to a leftward optical deviation was responsible for a shift in bisection toward the high numbers (i.e., to the right) (Loftus et al., 2008) that could be compared to a mild neglect-like behavior (Vuilleumier et al., 2004; Zorzi et al., 2002, 2006). The mental alphabetic line has also a left-to-right organization with early letters on the left side and later letters on the right side of space (Gevers et al., 2003; Zorzi et al., 2006). Normal subjects misbisect the mental distance toward early letters (i.e., to the left) (Zorzi et al., 2006; Nicholls and Loftus, 2007). Adaptation to a leftward optical deviation produces a shift in bisection toward the later letters (i.e., to the right) (Nicholls et al., 2008) that could be compared to a mild neglect-like behavior (Gevers et al., 2003; Zorzi et al., 2006). Cognitive after-effects also concern body representation. The analysis of the center of pressure (point of application of the ground reaction force vector) is a useful but indirect tool to assess the internal model of the body (Gurfinkel and Levick, 1991). Adaptation to a leftward optical deviation produced a rightward shift of the center of pressure in an eyes closed condition which correlated negatively with a counterclockwise estimation of the visual vertical (encoded within an egocentric frame of reference) (Michel et al., 2003b). These results on posture and subjective visual vertical are similar to mild symptoms following right brain lesion and more particularly neglect manifestations (Bohannon et al., 1986; Brandt et al., 1994; Rode et al., 1997, 1998; Kerkhoff, 1999; Tilikete et al., 2001). Altogether, prism adaptation affects a supramodal level of space representation in both explicit and non-explicit spatial tasks.
We could mention here that prism adaptation affects also spatial remapping that enables the construction of a stable representation of the visual environment despite constantly changing retinal images. Prism adaptation to a leftward optical deviation induces impairment in spatial remapping for left visual field targets in the double-step saccade paradigm (Bultitude et al., 2013c). These after-effects could be viewed as mild neglect behavior (Pisella et al., 2011).
After-Effects of Prism Adaptation in Attention and Hierarchical Processing
Because space representation depends on orientation of attention (e.g., Milner et al., 1992), the rightward representational after-effects described above could be partly explained by a redistribution of spatial attention to the detriment of the left space. Prism adaptation affects covert attention (Striemer et al., 2006) and has lateralised effects on spatial attention. Judgment of luminance (grayscales task) requires a forced choice judgment between two mirror-reversed luminance gradients. Participants usually select the stimulus that is darker on the left despite the fact that both stimuli are equiluminant (Nicholls et al., 1999; Okubo and Nicholls, 2006). This leftward bias is reversed following adaptation to a leftward optical deviation (Loftus et al., 2009b) mimicking neglect-like behavior in grayscales (Sarri et al., 2011).
The influence of prism adaptation extends also to hierarchical processing as first demonstrated by Bultitude and Woods (2010). When healthy participants are presented with figures in which small letters are arranged to form a large letter (Navon, 1977), they are faster to identify the global-level than the local-level information, and have difficulty ignoring global information when identifying the local level. After adaptation to a leftward optical deviation, there was a significant reduction in global interference similar to the processing bias demonstrated in patients with right temporo-parietal junction lesions (Bultitude et al., 2009). Reed and Dassonville (2014) demonstrated that adaptation to a leftward optical deviation increased the susceptibility to a subset of visual illusions known to be driven by local contextual processing. However, adaptation failed to influence performance in the composite face task that is supposed to evaluate the automatic global-level processing of faces (Bultitude et al., 2013a). Negative results were also observed on spatial attention in space-based or object-based attention (Bultitude et al., 2013b), in a temporal order judgment task (Berberovic et al., 2004), in saccade latencies or antisaccade errors (Nijboer et al., 2010) and in visual search (Morris et al., 2004; Saevarsson et al., 2009). Even if a lack of sensitivity cannot be excluded for several tasks, these negative results could be explained by the absence of pseudoneglect behavior in baseline performance. It has been proposed that any aspects of performance that have been altered by prism adaptation are ones for which the behavior is already biased toward pseudoneglect (Nijboer et al., 2010; Bultitude et al., 2013b) (see Paragraph 1). Therefore, the influence of prism adaptation could be viewed as reducing pseudoneglect or inversing pseudoneglect to produce mild neglect.
Why aren’t Cognitive After-Effects Explained by Sensorimotor After-Effects?
The occurrence of cognitive after-effects is even more interesting when considering that the development of prism adaptation relies on active motor behavior and that cognitive after-effects cannot be explained in terms of sensorimotor after-effects. Several arguments could be presented here. (1) If cognitive after-effects were explained by sensorimotor after-effects they would be mainly observed in tasks involving visuo-manual coordination. On the contrary, they are shown in tasks requiring verbal responses (Berberovic and Mattingley, 2003; Michel et al., 2003a; Loftus et al., 2008, 2009b; Nicholls et al., 2008; Nijboer et al., 2010; Schintu et al., 2014). (2) If cognitive after-effects were explained by sensorimotor after-effects the amplitude of the bias in bisection task would be independent of the spatial location because sensorimotor after-effects generalize homogeneously over space (Bedford, 1989). The bias would have also the same amplitude irrespective of the length of the line because relative position coding is not altered by wedge prisms (Redding and Wallace, 1996). On the contrary, line bisection bias is greater for left-sided locations than for right sided-locations and it increases with the line length (Michel et al., 2003a). (3) If cognitive after-effects were explained by sensorimotor after-effects they would be symmetric in amplitude following exposure to left and right optical deviations (Cohen, 1967; Loftus et al., 2008; Michel et al., 2003b, 2008; Schintu et al., 2014). On the contrary, cognitive after-effects on pseudoneglect behavior occur only following adaptation to a leftward optical deviation (Colent et al., 2000; Michel et al., 2003b; Loftus et al., 2008, 2009b; Nicholls et al., 2008; Bultitude and Woods, 2010; Goedert et al., 2010) (4) If cognitive after-effects result from sensorimotor after-effects they could be partly explained by visual after-effects. Prism adaptation is responsible for visual displacement of the gaze in the direction of the optical deviation during and after prism exposure (e.g., Wallace et al., 1973) due to eye muscle potentiation (Ebenholtz, 1974) and visual recalibration (Craske, 1975; Craske and Crawshaw, 1975). Because line bisection performance is biased toward the start location of the scanning direction (Brodie and Pettigrew, 1996; Chokron et al., 1998) a leftward bias could be expected after adaptation to a leftward optical deviation. On the contrary, a rightward bias is observed in line bisection (e.g., Colent et al., 2000; Striemer and Danckert, 2010) and in ocular exploration (Ferber and Murray, 2005) showing a reorganization of the visual functions that cannot be explained by visual after-effects. (5) If cognitive after-effects were explained by sensorimotor after-effects there would be a correlation between the amplitude of sensorimotor and cognitive after-effects. On the contrary, all studies analyzing the link between sensorimotor and cognitive after-effects showed no correlation (Berberovic and Mattingley, 2003; Girardi et al., 2004; Fortis et al., 2011; Herlihey et al., 2012; Guinet and Michel, 2013; Schintu et al., 2014).
Even if cognitive after-effects cannot be directly explained by sensorimotor after-effects, their occurrence strictly depends on the development of adaptation (spatial realignment) which needs active pointing movements during prism exposure (Michel et al., 2003a). Furthermore the spatial realignment must be strong enough (by using at least 10° optical deviation) to observe cognitive after-effects (Michel and Cruz, 2015). Nevertheless, the attempt to increase cognitive after-effects by combining neck muscle vibration with prism adaptation to increase the misperception of the target in the direction of the prismatic shift is unfruitful in healthy individuals (Guinet and Michel, 2013).
Sensorimotor and Cognitive After-Effects: Where is the Boundary?
The term ‘cognitive’ refers to the fact that effects take place beyond the usual framework of compensatory sensorimotor after-effects and involves mental abilities. Cognitive after-effects are mainly assessed by ‘paper-pencil’ tests or need verbal responses as manual line bisection or mental number bisection, respectively. They result from higher cognitive processes involved in judgment and comparison. In contrast, sensorimotor after-effects are exclusively shown in tasks assessing sensorimotor coordination as visuo-manual open-loop pointing. They result from adaptive changes in perception and motor command. Nevertheless, under certain circumstances, when a motor response is required for a cognitive task, both types of after-effects can coexist. This could be the case for the manual line bisection but the use of slow movements under visual guidance to set the bisection mark abolishes any sensorimotor influence (Redding and Wallace, 1996). The absence of correlation between cognitive and sensorimotor after-effects indicates that sensorimotor after-effects do not influence cognitive responses (see Paragraph 3). On the contrary, goal-oriented locomotion to a memorized visual target allows the coexistence of both types of after-effects because it involves memorized representation of a target in space for a few seconds (before and during the displacement) which favors the appearance of representational after-effects in far space (Michel et al., 2008). Moreover, as mentioned in Paragraph 3, the optical deviation used to produce after-effects is to consider. Cognitive after-effects are asymmetric whereas sensorimotor after-effects are symmetric.
From Pseudoneglect to Neglect-Like Behavior: How is it Possible?
Attempts to produce neglect in normals are based on the specialization of the human right hemisphere for visuo-spatial functions (e.g., Benton and Tranel, 1993). Interhemispheric changes to the detriment of the right hemisphere (or in favor of the left hemisphere) produce a mild neglect-like behavior or reduce pseudoneglect. For clarity and conciseness, only examples from line bisection studies are presented here. Leftward pseudoneglect bias in line bisection decreases when the right hand (versus left hand) is used (Scarisbrick et al., 1987; Fukatsu et al., 1990; Brodie and Pettigrew, 1996; Jewell and McCourt, 2000), when lines are located in right hemispace (Reuter-Lorenz et al., 1990; Luh, 1995; McCourt and Jewell, 1999) or when attention is oriented to the right extremity of the line (Milner et al., 1992; Harvey et al., 2000). Aging is also characterized by hemispheric changes. Faster aging of the right hemisphere (Meudell and Greenhalgh, 1987; Robinson and Kertzman, 1990) or reduced hemispheric asymmetry with aging (Dolcos et al., 2002; Reuter-Lorenz, 2002; Cabeza et al., 2004), may be responsible for a rightward bias in line bisection (Fujii et al., 1995; Schmitz and Peigneux, 2011; Benwell et al., 2014). Direct modulation of the cerebral activity by using transcranial magnetic stimulation (TMS) or transcranial direct current stimulation (tDCS) produces also neglect-like symptoms (Sack, 2010). The use of repetitive TMS over right frontal and right posterior parietal cortices produces a rightward neglect-like bias in line bisection (Fierro et al., 2000, 2001; Brighina et al., 2002; Ellison et al., 2004; Bjoertomt et al., 2009), in mental number line (Göbel et al., 2006) or in visual target detection (Thut et al., 2005; Muggleton et al., 2006). When right cathodal (hyperpolarization) and left anodal (depolarization) tDCS were simultaneously applied over homolog posterior parietal cortices or when only right cathodal tDCS was used, a rightward bias in landmark task was shown (Giglia et al., 2011; Benwell et al., 2015). Interestingly enough, when neglect-like bias was produced during TMS over the right parietal cortex, functional imaging studies showed a decreased activity within the site of stimulation and in interconnected right hemisphere structures and even enhanced BOLD signal in the left parietal and visual cortices (Sack et al., 2007; Heinen et al., 2011; Ricci et al., 2012).
Therefore, interhemispheric imbalance to the detriment of the right parietal cortex may explain prism-induced cognitive after-effects (Michel, 2006). Studies in brain damaged patients and healthy individuals underline the involvement of the parieto-cerebellar network in the development of adaptation (Clower et al., 1996; Pisella et al., 2005; Luauté et al., 2006, 2009; Danckert et al., 2008; Chapman et al., 2010; Crottaz-Herbette et al., 2014). The temporal cortex, involved during realignment, might also account for some of cognitive after-effects (Luauté et al., 2009). Otherwise, the hand used during prism exposure may have a potential influence on the hemispheric imbalance following adaptation. Except two studies (Michel et al., 2008; Reed and Dassonville, 2014) using both hands for visuo-manual pointings during prism exposure, the right dominant hand (involving the left hemisphere) is always used.
Conclusion
Prism adaptation is undoubtedly a fascinating phenomenon that urges us to revisit our conception of sensorimotor plasticity and questions us on the reciprocal relations between cognition and action. Prism adaptation is a powerful non-invasive method for neglect rehabilitation (e.g., Rossetti and Rode, 2002; Rode et al., 2015) that is able to mirror neglect in normal. Nevertheless the neural substrate of after-effects during a cognitive task following prism adaptation to a leftward optical deviation (conditions known to express neglect-like behavior) has not yet been studied in healthy individuals. Furthermore, the nature of the after-effects needs to be further investigated because it does not limit to sensorimotor and cognitive domains (e.g., Sumitani et al., 2007).
Conflict of Interest Statement
The author declares that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
References
Bedford, L. B. (1989). Constraints on learning new mappings between perceptual dimensions. J. Exp. Psychol. Hum. Percept. Perform. 15, 232–248. doi: 10.1037/0096-1523.15.2.232
Benton, A., and Tranel, D. (1993). “Visuoperceptual, Visuospatial, and visuoconstructive disorders,” in Clinical Neuropsychology, eds K. M. Heilman and E. Valensteinn (New York, NY: Oxford University Press), 165–213.
Benwell, C. S., Learmonth, G., Miniussi, C., Harvey, M., and Thut, G. (2015). Non-linear effects of transcranial direct current stimulation as a function of individual baseline performance: evidence from biparietal tDCS influence on lateralized attention bias. Cortex 69, 152–165. doi: 10.1016/j.cortex.2015.05.007
Benwell, C. S., Thut, G., Grant, A., and Harvey, M. (2014). A rightward shift in the visuospatial attention vector with healthy aging. Front. Aging Neurosci. 10:113. doi: 10.3389/fnagi.2014.00113
Berberovic, N., and Mattingley, J. B. (2003). Effects of prismatic adaptation on judgements of spatial extent in peripersonal and extrapersonal space. Neuropsychologia 41, 493–503. doi: 10.1016/S0028-3932(02)00090-8
Berberovic, N., Pisella, L., Morris, A. P., and Mattingley, J. B. (2004). Prismatic adaptation reduces biased temporal order judgements in spatial neglect. Neuroreport 15, 1199–1204. doi: 10.1097/00001756-200405190-00024
Berti, A., Smania, N., RabuVetti, M., Ferrarin, M., Spinazzola, L., D’Amico, A., et al. (2002). Coding of far and near space during walking in neglect patients. Neuropsychology 16, 390–399. doi: 10.1037/0894-4105.16.3.390
Bjoertomt, O., Cowey, A., and Walsh, V. (2009). Near space functioning of the human angular and supramarginal gyri. J. Neuropsychol. 3, 31–43. doi: 10.1348/174866408X394604
Bohannon, R. W., Smith, M. B., and Larkin, P. A. (1986). Relationship between independent sitting balance and side of hemiparesis. Phys. Ther. 66, 944–945.
Brandt, T., Dieterich, M., and Danek, A. (1994). Vestibular cortex lesions affect the perception of verticality. Ann. Neurol. 35, 403–412. doi: 10.1002/ana.410350406
Brighina, F., Bisiach, E., Piazza, A., Oliveri, M., La Bua, V., Daniele, O., et al. (2002). Perceptual and response bias in visuospatial neglect due to frontal and parietal repetitive transcranial magnetic stimulation in normal subjects. Neuroreport 13, 2571–2575. doi: 10.1097/00001756-200212200-00038
Brodie, E. E., and Pettigrew, L. E. (1996). Is left always right? Directional deviations in visual line bisection as a function of hand and initial scanning direction. Neuropsychologia 34, 467–470.
Bultitude, J. H., Downing, P. E., and Rafal, R. D. (2013a). Prism adaptation does not alter configural processing of faces. F1000Research 2, 215. doi: 10.12688/f1000research.2-215.v1
Bultitude, J. H., List, A., and Aimola Davies, A. M. (2013b). Prism adaptation does not alter object-based attention in healthy participants. F1000Research 2, 232. doi: 10.12688/f1000research.2-232.v1
Bultitude, J. H., Van der Stigchel, S., and Nijboer, T. C. (2013c). Prism adaptation alters spatial remapping in healthy individuals: evidence from double-step saccades. Cortex 49, 759–770. doi: 10.1016/j.cortex.2012.01.008
Bultitude, J. H., Rafal, R. D., and List, A. (2009). Prism adaptation reverses the local processing bias in patients with right temporo-parietal junction lesions. Brain 132, 1669–1677. doi: 10.1093/brain/awp096
Bultitude, J. H., and Woods, J. M. (2010). Adaptation to leftward-shifting prisms reduces the global processing bias of healthy individuals. Neuropsychologia 48, 1750–1756. doi: 10.1016/j.neuropsychologia.2010.02.024
Cabeza, R., Daselaar, S. M., Dolcos, F., Prince, S. E., Budde, M., and Nyberg, L. (2004). Task-independent and task-specific age effects on brain activity during working memory, visual attention and episodic retrieval. Cereb. Cortex 14, 364–375. doi: 10.1093/cercor/bhg133
Chapman, H. L., Eramudugolla, R., Gavrilescu, M., Strudwick, M. W., Loftus, A., Cunnington, R., et al. (2010). Neural mechanisms underlying spatial realignment during adaptation to optical wedge prisms. Neuropsychologia 48, 2595–2601. doi: 10.1016/j.neuropsychologia.2010.05.006
Chokron, S., Bartolomeo, P., Perenin, M. T., Helft, G., and Imbert, M. (1998). Scanning direction and line bisection: a study of normal subjects and unilateral neglect patients with opposite reading habits. Brain Res. Cogn. Brain Res. 7, 173–178. doi: 10.1016/S0926-6410(98)00022-6
Clower, D. M., Hoffman, J. M., Votaw, J. R., Faber, T. L., Woods, R. P., and Alexander, G. E. (1996). Role of posterior parietal cortex in the recalibration of visually guided reaching. Nature 383, 618–621. doi: 10.1038/383618a0
Cohen, M. M. (1967). Continuous versus terminal visual feedback in prism aftereVects. Percept. Mot. Skills 24, 1295–1302. doi: 10.2466/pms.1967.24.3c.1295
Colent, C., Pisella, L., Bernieri, C., Rode, G., and Rossetti, Y. (2000). Cognitive bias induced by visuo-motor adaptation to prisms: a simulation of unilateral neglect in normal individuals? Neuroreport 11, 1899–1902. doi: 10.1097/00001756-200006260-00019
Craske, B. (1975). “A current view of the processes and mechanisms of prism adaptation,” in Aspects of Neuronal Plasticity, eds F. Vital-Durand and M. Jeannerod (Paris: INSERM), 125–138.
Craske, B., and Crawshaw, M. (1975). Oculomotor adaptation to prism is not simply a muscle potentiation effect. Percept. Psychophys. 18, 105–106. doi: 10.3758/BF03204095
Crottaz-Herbette, S., Fornari, E., and Clarke, S. (2014). Prismatic adaptation changes visuospatial representation in the inferior parietal lobule. J. Neurosci. 34, 11803–11811. doi: 10.1523/JNEUROSCI.3184-13.2014
Danckert, J., Ferber, S., and Goodale, M. A. (2008). Direct effects of prismatic lenses on visuomotor control: an event-related functional MRI study. Eur. J. Neurosci. 28, 1696–1704. doi: 10.1111/j.1460-9568.2008.06460.x
Dehaene, S., Bossini, S., and Giraux, P. (1993). The mental representation of parity and number magnitude. J. Exp. Psychol. Gen. 122, 371–396. doi: 10.1037/0096-3445.122.3.371
Dolcos, F., Rice, H. J., and Cabeza, R. (2002). Hemispheric asymmetry and aging: right hemisphere decline or asymmetry reduction. Neurosci. Biobehav. Rev. 26, 819–825. doi: 10.1016/S0149-7634(02)00068-4
Ebenholtz, S. M. (1974). The possible role of eye-muscle potentiation in several forms of prism adaptation. Perception 3, 477–485. doi: 10.1068/p030477
Ellison, A., Schindler, I., Pattison, L. L., and Milner, A. D. (2004). An exploration of the role of the superior temporal gyrus in visual search and spatial perception using TMS. Brain 127, 2307–2315. doi: 10.1093/brain/awh244
Ferber, S., and Murray, L. J. (2005). Are perceptual judgments dissociated from motor processes? A prism adaptation study. Brain Res. Cogn. Brain Res. 23, 453–456. doi: 10.1016/j.cogbrainres.2004.11.007
Fierro, B., Brighina, F., Oliveri, M., Piazza, A., La Bua, V., Buffa, D., et al. (2000). Contralateral neglect induced by right posterior parietal rTMS in healthy subjects. Neuroreport 11, 1519–1521. doi: 10.1097/00001756-200005150-00030
Fierro, B., Brighina, F., Piazza, A., Oliveri, M., and Bisiach, E. (2001). Timing of right parietal and frontal cortex activity in visuo-spatial perception: a TMS study in normal individuals. Neuroreport 12, 2605–2607. doi: 10.1097/00001756-200108080-00062
Fink, G. R., Marshall, J. C., Weiss, P. H., and Zilles, K. (2001). The neural basis of vertical and horizontal line bisection judgments: an fMRI study of normal volunteers. Neuroimage 14, 59–67. doi: 10.1006/nimg.2001.0819
Fortis, P., Goedert, K. M., and Barrett, A. M. (2011). Prism adaptation differently affects motor-intentional and perceptual-attentional biases in healthy individuals. Neuropsychologia 49, 2718–2727. doi: 10.1016/j.neuropsychologia.2011.05.020
Fujii, T., Fukatsu, R., Yamadori, A., and Kimura, I. (1995). Effect of age on the line bisection test. J. Clin. Exp. Neuropsychol. 17, 941–944. doi: 10.1080/01688639508402443
Fukatsu, R., Fujii, T., Kimura, I., Saso, S., and Kogure, K. (1990). Effects of hand and spatial conditions on visual line bisection. Tohoku J. Exp. Med. 161, 329–333. doi: 10.1620/tjem.161.329
Gevers, W., Reynvoet, B., and Fias, W. (2003). The mental representation of sequences is spatially organized. Cognition 87, 87–95. doi: 10.1016/S0010-0277(02)00234-2
Giglia, G., Mattaliano, P., Puma, A., Rizzo, S., Fierro, B., and Brighina, F. (2011). Neglect-like effects induced by tDCS modulation of posterior parietal cortices in healthy subjects. Brain Stimul. 4, 294–299. doi: 10.1016/j.brs.2011.01.003
Girardi, M., McIntosh, R. D., Michel, C., Vallar, G., and Rossetti, Y. (2004). Sensorimotor effects on central space representation: prism adaptation influences haptic and visual representations in normal subjects. Neuropsychologia 42, 1477–1487. doi: 10.1016/j.neuropsychologia.2004.03.008
Göbel, S. M., Calabria, M., Farnè, A., and Rossetti, Y. (2006). Parietal rTMS distorts the mental number line: simulating ‘spatial’ neglect in healthy subjects. Neuropsychologia 44, 860–868. doi: 10.1016/j.neuropsychologia.2005.09.007
Goedert, K. M., Leblanc, A., Tsai, S. W., and Barrett, A. M. (2010). Asymmetrical effects of adaptation to left– and right-shifting prisms depends on pre-existing attentional biases. J. Int. Neuropsychol. Soc. 16, 795–804. doi: 10.1017/S1355617710000597
Guinet, M., and Michel, C. (2013). Prism adaptation and neck muscle vibration in healthy individuals: are two methods better than one? Neuroscience 254, 443–451. doi: 10.1016/j.neuroscience.2013.08.067
Gurfinkel, V. S., and Levick, Y. S. (1991). “Perceptual and automatic aspects of the postural body scheme,” in Brain and Space, ed. J. Paillard (Oxford: Oxford University Press), 147–162.
Halligan, P. W. (1995). Drawing attention to neglect: the contribution of line bisection. Psychologist 8, 257–264.
Harvey, M., Pool, T. D., Roberson, M. J., and Olk, B. (2000). Effects of visible and invisible cueing procedures on perceptual judgments in young and elderly subjects. Neuropsychologia 38, 22–31. doi: 10.1016/S0028-3932(99)00055-X
Heilman, K., Watson, R. T., and Valenstein, E. (1993). “Neglect and related disorders,” in Clinical Neuropsychology, eds K. M. Heilman and E. Valenstein (New York, NY: Oxford University Press), 279–336.
Heinen, K., Ruff, C. C., Bjoertomt, O., Schenkluhn, B., Bestmann, S., Blankenburg, F., et al. (2011). Concurrent TMS-fMRI reveals dynamic interhemispheric influences of the right parietal cortex during exogenously cued visuospatial attention. Eur. J. Neurosci. 33, 991–1000. doi: 10.1111/j.1460-9568.2010.07580.x
Herlihey, T. A., Black, S. E., and Ferber, S. (2012). Terminal, but not concurrent prism exposure produces perceptual aftereffects in healthy young adults. Neuropsychologia 50, 2789–2795. doi: 10.1016/j.neuropsychologia.2012.08.009
Jacquin-Courtois, S., O’Shea, J., Luauté, J., Pisella, L., Revol, P., Mizuno, K., et al. (2013). Rehabilitation of spatial neglect by prism adaptation: a peculiar expansion of sensorimotor after-effects to spatial cognition. Neurosci. Biobehav. Rev. 37, 594–609. doi: 10.1016/j.neubiorev.2013.02.007
Jewell, G., and McCourt, M. E. (2000). Pseudoneglect: a review and meta-analysis of performance factors in line bisection tasks. Neuropsychologia 38, 93–110. doi: 10.1016/S0028-3932(99)00045-7
Kerkhoff, G. (1999). Multimodal spatial orientation deficits in leftsided visual neglect. Neuropsychologia 37, 1387–1407. doi: 10.1016/S0028-3932(99)00031-7
Kornheiser, A. S. (1976). Adaptation to laterally displaced vision: a review. Psychol. Bull. 83, 783–816. doi: 10.1037/0033-2909.83.5.783
Loftus, A. M., Nicholls, M. E., Mattingley, J. B., and Bradshaw, J. L. (2008). Left to right: representational biases for numbers and the effect of visuomotor adaptation. Cognition 107, 1048–1058. doi: 10.1016/j.cognition.2007.09.007
Loftus, A. M., Nicholls, M. E., Mattingley, J. B., Chapman, H. L., and Bradshaw, J. L. (2009a). Pseudoneglect for the bisection of mental number lines. Q. J. Exp. Psychol. 62, 925–945. doi: 10.1080/17470210802305318
Loftus, A. M., Vijayakumar, N., and Nicholls, M. E. (2009b). Prism adaptation overcomes pseudoneglect for the greyscales task. Cortex 45, 537–543. doi: 10.1016/j.cortex.2007.12.011
Longo, M. R., and Lourenco, S. F. (2007). Spatial attention and the mental number line: evidence for characteristic biases and compression. Neuropsychologia 4, 1400–1407. doi: 10.1016/j.neuropsychologia.2006.11.002
Luauté, J., Michel, C., Rode, G., Pisella, L., Jacquin-Courtois, S., Costes, N., et al. (2006). Functional anatomy of the therapeutic effects of prism adaptation on left neglect. Neurology 66, 1859–1867. doi: 10.1212/01.wnl.0000219614.33171.01
Luauté, J., Schwartz, S., Rossetti, Y., Spiridon, M., Rode, G., Boisson, D., et al. (2009). Dynamic changes in brain activity during prism adaptation. J. Neurosci. 29, 169–178. doi: 10.1523/JNEUROSCI.3054-08.2009
Luh, K. E. (1995). Line bisection and perceptual asymmetries in normal individuals: what you see os not what you get. Neuropsychology 9, 435–448. doi: 10.1037/0894-4105.9.4.435
McCourt, M. E., and Jewell, G. (1999). Visuospatial attention in line bisection: stimulus modulation of pseudoneglect. Neuropsychologia 37, 843–855. doi: 10.1016/S0028-3932(98)00140-7
McIntosh, R. D., Rossetti, Y., and Milner, A. D. (2002). Prism adaptation improves chronic visual and haptic neglect: a single case study. Cortex 38, 309–320. doi: 10.1016/S0010-9452(08)70662-2
Meudell, P. R., and Greenhalgh, M. (1987). Age related differences inleft and right hand skill and in visuo-spatial performance: their possible relationships to the hypothesis that the right hemisphere ages more rapidly than the left. Cortex 23, 431–445. doi: 10.1016/S0010-9452(87)80005-9
Michel, C. (2006). Simulating unilateral neglect in normals: myth or reality? Restor. Neurol. Neurosci. 24, 419–430.
Michel, C., and Cruz, R. (2015). Prism adaptation power on spatial cognition: adaptation to different optical deviations in healthy individuals. Neurosci. Lett. 590, 145–149. doi: 10.1016/j.neulet.2015.02.001
Michel, C., Pisella, L., Halligan, P. W., Luaute, J., Rode, G., Boisson, D., et al. (2003a). Simulating unilateral neglect in normals using prism adaptation: implications for theory. Neuropsychologia 4, 25–39. doi: 10.1016/S0028-3932(02)00135-5
Michel, C., Rossetti, Y., Rode, G., and Tilikete, C. (2003b). After-effects of visuo-manual adaptation to prisms on body posture in normal subjects. Exp. Brain Res. 148, 219–226.
Michel, C., Vernet, P., Courtine, G., Ballay, Y., and Pozzo, T. (2008). Asymmetrical after-effects of prism adaptation during goal oriented locomotion. Exp. Brain Res. 18, 259–268. doi: 10.1007/s00221-007-1152-4
Milner, A. D., Brechmann, M., and Pagliarini, L. (1992). To halve and to halve not: an analysis of line bisection judgements in normal subjects. Neuropsychologia 30, 515–526. doi: 10.1016/0028-3932(92)90055-Q
Morris, A. P., Kritikos, A., Berberovic, N., Pisella, L., Chambers, C. D., and Mattingley, J. B. (2004). Prism adaptation and spatial attention: a study of visual search in normals and patients with unilateral neglect. Cortex 40, 703–721. doi: 10.1016/S0010-9452(08)70166-7
Muggleton, N. G., Postma, P., Moutsopoulou, K., Nimmo-Smith, I., Marcel, A., and Walsh, V. (2006). TMS over right posterior parietal cortex induces neglect in a scene-based frame of reference. Neuropsychologia 44, 1222–1229. doi: 10.1016/j.neuropsychologia.2005.10.004
Navon, D. (1977). Forest before trees: the precedence of global features in visual perception. Cogn. Psychol. 9, 353–383. doi: 10.1016/0010-0285(77)90012-3
Newport, R., and Schenk, T. (2012). Prisms and neglect: what have we learned? Neuropsychologia 50, 1080–1091. doi: 10.1016/j.neuropsychologia.2012.01.023
Nicholls, M. E. R., Bradshaw, J. L., and Mattingley, J. B. (1999). Free-viewing perceptual asymmetries for the judgement of shade, numerosity and size. Neuropsychologia 37, 307–314. doi: 10.1016/S0028-3932(98)00074-8
Nicholls, M. E. R., Kamer, A., and Loftus, A. M. (2008). Pseudoneglect for mental alphabet lines is affected by prismatic adaptation. Exp. Brain Res. 191, 109–115. doi: 10.1007/s00221-008-1502-x
Nicholls, M. E. R., and Loftus, A. M. (2007). Pseudoneglect and neglect for mental alphabet lines. Brain Res. 1152, 130–138. doi: 10.1016/j.brainres.2007.03.036
Nijboer, T., Vree, A., Dijkerman, C., and Van der Stigchel, S. (2010). Prism adaptation influences perception but not attention: evidence from antisaccades. Neuroreport 21, 386–389. doi: 10.1097/WNR.0b013e328337f95f
Okubo, M., and Nicholls, M. E. R. (2006). A stimulus-dependent dissociation between the cerebral hemispheres under free-viewing conditions. Exp. Brain Res. 172, 49–56. doi: 10.1007/s00221-005-0303-8
Pisella, L., Alahyane, N., Blangero, A., Thery, F., Blanc, S., and Pelisson, D. (2011). Right-hemispheric dominance for visual remapping in humans. Philos. Trans. R. Soc. Lond. B Biol. Sci. 366, 572–585. doi: 10.1098/rstb.2010.0258
Pisella, L., Rossetti, Y., Michel, C., Rode, G., Boisson, D., Pelisson, D., et al. (2005). Ipsidirectional impairment of prism adaptation after unilateral lesion of anterior cerebellum. Neurology 65, 150–152. doi: 10.1212/01.wnl.0000167945.34177.5e
Redding, G. M., and Wallace, B. (1996). Adaptive spatial alignment and strategic perceptual-motor control. J. Exp. Psychol. Hum. Percept. Perform. 22, 379–394. doi: 10.1037/0096-1523.22.2.379
Reed, S. A., and Dassonville, P. (2014). Adaptation to leftward-shifting prisms enhances local processing in healthy individuals. Neuropsychologia 56, 418–427. doi: 10.1016/j.neuropsychologia.2014.02.012
Reuter-Lorenz, P. (2002). New visions of the aging mind and brain. Trends Cogn. Sci. 6, 394. doi: 10.1016/S1364-6613(02)01957-5
Reuter-Lorenz, P. A., Kinsbourne, M., and Moscovitch, M. (1990). Hemispheric control of spatial attention. Brain Cogn. 12, 240–266. doi: 10.1016/0278-2626(90)90018-J
Ricci, R., Salatino, A., Li, X., Funk, A. P., Logan, S. L., Mu, Q., et al. (2012). Imaging the neural mechanisms of TMS neglect-like bias in healthy volunteers with the interleaved TMS/fMRI technique: preliminary evidence. Front. Hum. Neurosci. 6:326. doi: 10.3389/fnhum.2012.00326
Robertson, I. H., Tegner, R., Goodrich, S. J., and Wilson, C. (1994). Walking trajectory and hand movements in unilateral left neglect: a vestibular hypothesis. Neuropsychologia 32, 1495–1502. doi: 10.1016/0028-3932(94)90121-X
Robinson, D. L., and Kertzman, C. (1990). Visuospatial attention: effect sof age, gender and spatial reference. Neuropsychologia 28, 291–301. doi: 10.1016/0028-3932(90)90022-G
Rode, G., Lacour, S., Jacquin-Courtois, S., Pisella, L., Michel, C., Revol, P., et al. (2015). Long-term sensorimotor and therapeutical effects of a mild regime of prism adaptation in spatial neglect. A double-blind RCT essay. Ann. Phys. Rehabil. Med. 58, 40–53. doi: 10.1016/j.rehab.2014.10.004
Rode, G., Tiliket, C., and Boisson, D. (1997). Predominance of postural imbalance in left hemiparetic patients. Scand. J. Rehabil. Med. 29, 11–16.
Rode, G., Tiliket, C., Charlopain, P., and Boisson, D. (1998). Postural asymmetry reduction by vestibular caloric stimulation in left hemiparetic patients. Scand. J. Rehabil. Med. 30, 9–14. doi: 10.1080/003655098444264
Rossetti, Y., and Rode, G. (2002). “Reducing spatial neglect by visual and other sensory manipulations: non-cognitive (physiological) routes to the rehabilitation of a cognitive disorder,” in The Cognitive and Neural Bases of Spatial Neglect, eds H. O. Karnath, A. D. Milner, and G. Vallar (New York, NY: Oxford University Press), 375–396.
Rossetti, Y., Rode, G., Pisella, L., Farne, A., Li, L., Boisson, D., et al. (1998). Prism adaptation to a rightward optical deviation rehabilitates left hemispatial neglect. Nature 395, 166–169. doi: 10.1038/25988
Sack, A. T. (2010). Using non-invasive brain interference as a tool for mimicking spatial neglect in healthy volunteers. Restor. Neurol. Neurosci. 28, 485–497. doi: 10.3233/RNN-2010-0568
Sack, A. T., Kohler, A., Bestmann, S., Linden, D. E., Dechent, P., Goebel, R., et al. (2007). Imaging the brain activity changes underlying impaired visuospatial judgments: simultaneous FMRI, TMS, and behavioral studies. Cereb. Cortex 17, 2841–2852. doi: 10.1093/cercor/bhm013
Saevarsson, S., Kristjánsson, A., Hildebrandt, H., and Halsband, U. (2009). Prism adaptation improves visual search in hemispatial neglect. Neuropsychologia 47, 717–725. doi: 10.1016/j.neuropsychologia.2008.11.026
Sarri, M., Greenwood, R., Kalra, L., and Driver, J. (2011). Prism adaptation does not change the rightward spatial preference bias found with ambiguous stimuli in unilateral neglect. Cortex 47, 353–366. doi: 10.1016/j.cortex.2010.01.006
Scarisbrick, D. J., Tweedy, J. R., and Kuslansky, G. (1987). Hand preference and performance effects on line bisection. Neuropsychologia 25, 695–699. doi: 10.1016/0028-3932(87)90061-3
Schintu, S., Pisella, L., Jacobs, S., Salemme, R., Reilly, K. T., and Farnè, A. (2014). Prism adaptation in the healthy brain: the shift in line bisection judgments is long lasting and fluctuates. Neuropsychologia 53, 165–170. doi: 10.1016/j.neuropsychologia.2013.11.013
Schmitz, R., and Peigneux, P. (2011). Age-related changes in visual pseudoneglect. Brain Cogn. 76, 382–389. doi: 10.1016/j.bandc.2011.04.002
Stratton, G. M. (1896). Some preliminary experiments on vision without inversion of the retinal image. Psychol. Rev. 3, 611–617. doi: 10.1037/h0072918
Striemer, C. L., and Danckert, J. (2010). Dissociating perceptual and motor effects of prismadaptation in neglect. Neuroreport 21, 436–441. doi: 10.1097/WNR.0b013e328338592f
Striemer, C., Sablatnig, J., and Danckert, J. (2006). Differential influences of prism adaptation on reflexive and voluntary covert attention. J. Int. Neuropsychol. Soc. 12, 337–349. doi: 10.1017/S1355617706060553
Sumitani, M., Rossetti, Y., Shibata, M., Matsuda, Y., Sakaue, G., Inoue, T., et al. (2007). Prism adaptation to optical deviation alleviates pathologic pain. Neurology 68, 128–133. doi: 10.1212/01.wnl.0000250242.99683.57
Thut, G., Nietzel, A., and Pascual-Leone, A. (2005). Dorsal posterior parietal rTMS affects voluntary orienting of visuospatial attention. Cereb. Cortex 15, 628–638. doi: 10.1093/cercor/bhh164
Tilikete, C., Rode, G., Rossetti, Y., Pichon, J., Ling, L., and Boisson, D. (2001). Prism adaptation to rightward optical deviation improves postural imbalance in left hemiparetic patients. Curr. Biol. 11, 1–20. doi: 10.1016/S0960-9822(01)00151-8
Vuilleumier, P., Ortigue, S., and Brugger, P. (2004). The number space and neglect. Cortex 40, 399–410. doi: 10.1016/S0010-9452(08)70134-5
Wallace, B., Melamed, L. E., and Kaplan, C. (1973). Movement and illumination factors in adaptation to viewing. Percept. Psychophys. 13, 164–168. doi: 10.3758/BF03214122
Zorzi, M., Priftis, K., Meneghello, F., Marenzi, R., and Umilta, C. (2006). The spatial representation of numerical and non-numerical sequences: evidence from neglect. Neuropsychologia 44, 1061–1067. doi: 10.1016/j.neuropsychologia.2005.10.025
Keywords: prism adaptation, cognition, after-effects, pseudoneglect, neglect
Citation: Michel C (2016) Beyond the Sensorimotor Plasticity: Cognitive Expansion of Prism Adaptation in Healthy Individuals. Front. Psychol. 6:1979. doi: 10.3389/fpsyg.2015.01979
Received: 25 September 2015; Accepted: 10 December 2015;
Published: 05 January 2016.
Edited by:
Luca Tommasi, Università degli Studi “G. d’Annunzio” Chieti – Pescara, ItalyReviewed by:
Igor Christian Schindler, University of Hull, UKGiorgia Committeri, Università degli Studi “G. d’Annunzio" Chieti – Pescara, Italy
Copyright © 2016 Michel. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
*Correspondence: Carine Michel, carine.michel@u-bourgogne.fr