Johansen-Berg, H

Maimon-Mor, RO

Makin, TR

Oxford University Research Archive

www.sciencedirect.comc o r t e x 9 5 ( 2 0 1 7 ) 1 6 9e1 7 1Available online atScienceDirectJournal homepage: www.elsevier.com/locate/cortexLetter to the editorPeri-hand space representation in the absence of ahand e Evidence from congenital one-handersRoni O. Maimon-Mor a, Heidi Johansen-Berg a and Tamar R. Makin a,b,*a FMRIB Centre, Nuffield Department of Clinical Neuroscience, University of Oxford, Oxford OX39DU, UnitedKingdomb Institute of Cognitive Neuroscience, University College London, London WC1N 3AZ, United Kingdoma r t i c l e i n f oArticle history:Received 3 February 2017Reviewed 5 April 2017Revised 12 June 2017Accepted 9 August 2017Published online 21 August 2017Keywords:Peripersonal spaceBody representationAmputeesNeuroimagingMultisensory integrationSpatial representation* Corresponding author. Institute of CognitivKingdom.E-mail address: t.makin@ucl.ac.uk (T.R. Mhttp://dx.doi.org/10.1016/j.cortex.2017.08.0160010-9452/© 2017 The Authors. Published byorg/licenses/by/4.0/).Here, we examined the representation of peri-(missing)-hand space (P[M]HS) in one-handers, by interrogating their PHSactivated when objects are approaching the missing hand. If,however, PHS network is defined by the zone for objectThe space immediately surrounding us is known to be rep-resented relative to our hands, i.e. in a hand-centred coordi-nate system (peri-hand space, PHS) (Graziano, Hu, & Gross,1997; for review see; Brozzoli, Makin, Cardinali, Holmes, &Farne, 2012). Individuals born without a hand (hereafter one-handers) manually interact with the world differently,potentially altering the representation of their near space.Previous behavioural research on PHS representation in one-handers and acquired amputees found evidence of a mild vi-suospatial bias against their missing hand side (Makin, Wilf,Schwartz, & Zohary, 2010), suggesting that hand loss im-pacts visual processing.e Neuroscience, Universiakin).Elsevier Ltd. This is an openetwork using functional neuroimaging. The PHS network iscomprised of several brain regions, most prominently: theanterior and posterior parts of the intraparietal sulcus (IPS), thelateral occipital cortex (LOC), the supramarginal gyrus and thepre-motor cortex (Brozzoli, Gentile, Bergouignan, & Ehrsson,2013; Brozzoli, Gentile, Petkova, & Ehrsson, 2011; Makin,Holmes, & Zohary, 2007). A subset of this network is sensitiveto visual features of the hand position, rather than its veridicalposition (e.g., LOC and posterior IPS) (Makin et al., 2007).If the PHS network is specifically anchored to the hand, thenthe absence of a hand should result in diminished P[M]HS rep-resentation (andpossiblyenhancedrepresentation inrelation tothe intact hand). Moreover, areas known to selectively respondto visual features of the hand (e.g., posterior IPS) should not bemanipulation (Brozzoli, Ehrsson, & Farne, 2014; Makin, Holmes,Brozzoli, & Farne, 2012), representation should be tied to theparticipant's ability to interact with objects, and anchored towhichever actuator supplements the missing hand function.Under this framework, diminished P[M]HS representationwould result from the reduced ability to interact with objects.We examined PHS representation in 10 one-handers bornwith one hand due to congenital upper-limb below-elbowdeficiency; Table S1 in the Supplementary Material. Wefurther compared PMHS with an additional group of below-elbow unilateral amputees (n ¼ 9) for control purposes.Within each functional run a 3D moving object appeared inone of two locations: either near or far from the participants'ty College London, 17 Queen Square, London, WC1N 3AZ, Unitedn access article under the CC BY license (http://creativecommons.Fig. 1 e (A) A schematic illustration of the experimental conditions. In each condition, a moving object was presented in oneof two positions, near or far. The participant maintained fixation between the positions throughout the experiment(Fixation point indicated by red cross-hairs; line of sight, via a mirror, indicted by dotted red line). Arm positions changedbetween conditions as follows: Baseline condition e both arms were retracted, Handless-arm condition e intact-armretracted and handless-arm extended, Intact-arm condition e intact-arm extended and handless arm retracted. (B) Visualselectivity for the space surrounding the handless or intact arms in one-handers. The hemisphere contralateral to the intacthand is presented on the left and the hemisphere contralateral to the missing hand on the right. Areas showing greaterdifferential near > far activity in handless-arm condition over baseline were found in both hemispheres and are presentedin an orange-yellow gradient (z values are indicated in the bottom). Areas showing greater differential near > far activity inintact-arm condition over baseline were found in the hemisphere contralateral to the intact hand only, and are presented inblack lines. Clusters are defined using family-wise-error-corrected cluster significance threshold of p < .05. UnthresholdedZ-maps can be found online at: https://neurovault.org/collections/2119/.c o r t e x 9 5 ( 2 0 1 7 ) 1 6 9e1 7 1170body, as used in previous studies (Brozzoli et al., 2011, 2013;Makin et al., 2007). In order to evaluate the PHS network of asingle hand the spatial relationship between the visual stimuliand participants' upper limbs differed across runs: (1)handless-arm visibly extended towards the near stimulus,intact hand retracted and (2) intact-arm visibly extended to-wards the near stimulus, handless-arm retracted (Fig. 1A, seeSupplementary Methods for further details). In addition, aseparate baseline run was acquired in which both arms wereretracted away from the visual stimuli. Each of these threeruns was repeated twice. To identify brain areas that showgreater activity to objects positioned close to the hand anear > far contrast was calculated within each of the armruns. To control for differences in visual features betweennear and far positions that are not PHS relevant, this wascontrasted with the near > far contrast of the baseline runs.Therefore, PHS network was identified for each arm using thecontrast [arm (near > far)] > [baseline (near > far)].We found strong and widespread activity in the PHSnetwork anchored to the handless-arm of one-handers (P[M]HS; Fig. 1B). In particular, differential activity was identified inPHS regions such as anterior IPS and supramarginal gyrusipsilaterally to the handless arm, but also in the posterior IPS(bilaterally) and LOC (ipsilaterally), thought to be sensitive tovisual features of hand position (Fig. 1B, Table S2). The P[M]HSactivity profile overlapped with PHS network activity for theintact hand (Black contour in Fig. 1B, Table S3) and wasconsistent with previous reports of PHS in individuals withtwo hands (Brozzoli et al., 2011; Makin et al., 2007). This sug-gests that spatial representation in those areas is anchored tothe position of the handless-arm, irrespective of the actualphysical absence of the hand itself.c o r t e x 9 5 ( 2 0 1 7 ) 1 6 9e1 7 1 171We next determined how one-handers' P[M]HS represen-tation compareswithanotherpopulationwithahand-loss.Wetherefore compared P[M]HS in one-handers and in acquiredamputees undergoing the same experimental procedure(Figure S1). While one-handers and amputees both have one-hand, they show important brain and behavioural differences(Makin et al., 2013) relevant for P[M]HS representation (seeSupplementary methods and discussion). For example, asdemonstrated by the current study cohort, acquired amputeesshow reduced functionality of their handless-arm in dailytasks compared to one-handers (ManneWhitney U ¼ 8.5,p ¼ .002). A group comparison for near > far contrast in thehandless-armcondition revealed increased activity in a subsetof PHS network in one handers, relative to acquired amputees(see Supplementary figure S2). This suggests that P[M]HS rep-resentationdoesnot automatically remap to thehandlessarm.Our main finding shows that the P[M]HS evoked activity ispresent in one-handers despite congenital hand-loss. Wesuggest that PHS network, normally representing the spacesurrounding the hand, can adapt to represent the space sur-rounding the handless-arm in the absence of a hand. Thisreanchoring of PHS in one handers, and the finding of greaterP[M]HS activity in one handers compared to amputees, can beinterpreted differently under two existing frameworks. First,considering the evidence for PHS as an interface for effector-centred representation, and the suggested remapping of PHSduring prosthesis (Canzoneri, Marzolla, Amoresano, Verni, &Serino, 2013) and tool use (Martel, Cardinali, Roy, & Farne,2016) the increased use of the handless arm in one-handersshould lead to a greater representation of P[M]HS in one-handers compared to acquired amputees. This interpreta-tion is consistent with recent findings showing that high dailyusage of the residual arm in one handers associates withincreased arm representation in the sensorimotor system(Hahamy et al., 2015, 2017). Alternatively, the reanchoring of P[M]HS representation to the arm (instead of the hand) mightonly be possible during the developmental period of the visualsystem (Wandell& Smirnakis, 2010), leading to greater P[M]HSactivity for congenital one-handers than for acquired ampu-tees. This interpretation introduces new considerations forthe ability of PHS representation to dynamically change. Sinceone-handers use their handless-arm to interact with objectsand experienced handlessness from early development, it isdifficult to determine which framework provides betterinterpretation to our results.AcknowledgmentsT.R.M. holds a Sir Henry Dale Fellowship jointly funded by theWellcome Trust and the Royal Society (Grant Number 104128/Z/14/Z). R.O.M.M. is supported by the Clarendon scholarshipand University College, Oxford. H.J.B. is a Wellcome TrustPrincipal Research Fellow (Grant number: 110027/Z/15/Z). Wethank our participants and Opcare for their help, AlonaCramer for her contribution in data collection and AlessandroFarne and Matan Mazor for their comments on the manu-script.We thank Jorge FernandezQuesada for his illustrations.The authors declare no conflict of interest.Supplementary dataSupplementary data related to this article can be found athttp://dx.doi.org/10.1016/j.cortex.2017.08.016.r e f e r e n c e sBrozzoli, C., Ehrsson, H. H., & Farne, A. (2014). Multisensoryrepresentation of the space near the hand: From perception toaction and interindividual interactions. The Neuroscientist,20(2), 122e135. http://dx.doi.org/10.1177/1073858413511153.Brozzoli, C., Gentile, G., Bergouignan, L., & Ehrsson, H. H. (2013). Ashared representation of the space near oneself and others inthe human premotor cortex. Current Biology, 23.Brozzoli, C., Gentile, G., Petkova, V. I., & Ehrsson, H. H. (2011). fMRIadaptation reveals a cortical mechanism for the coding ofspace near the hand. Journal of Neuroscience, 31(24), 9023e9031.http://dx.doi.org/10.1523/JNEUROSCI.1172-11.2011.Brozzoli, C., Makin, T. R., Cardinali, L., Holmes, N. P., & Farne, A.(2012). Peripersonal space: A multisensory interface for bodyeobjectinteractions. The neural bases of multisensory processes. Taylor &Francis: CRC Press.Canzoneri, E., Marzolla, M., Amoresano, A., Verni, G., & Serino, A.(2013). Amputation and prosthesis implantation shape bodyand peripersonal space representations. Scientific Reports,3(2844). http://dx.doi.org/10.1038/srep02844.Graziano, M. S. A., Hu, X. T., & Gross, C. G. (1997). Visuospatialproperties of ventral premotor cortex. Journal ofNeurophysiology, 77(5).Hahamy, A., Macdonald, S. N., van den Heiligenberg, F.,Kieliba, P., Emir, U., Malach, R., et al. (2017). Representation ofmultiple body parts in the missing-hand territory ofcongenital one-handers. Current Biology, 27(9), 1350e1355.http://dx.doi.org/10.1016/j.cub.2017.03.053.Hahamy, A., Sotiropoulos, S. N., Henderson Slater, D., Malach, R.,Johansen-Berg, H., & Makin, T. R. (2015). Normalisation ofbrain connectivity through compensatory behaviour, despitecongenital hand absence. eLife, 4. http://dx.doi.org/10.7554/eLife.04605.Makin, T. R., Cramer, A. O., Scholz, J., Hahamy, A., HendersonSlater, D., Tracey, I., et al. (2013). Deprivation-related and use-dependent plasticity go hand in hand. eLife, 2013, 1e15. http://dx.doi.org/10.7554/eLife.01273.01273.Makin, T. R., Holmes, N. P., Brozzoli, C., & Farne, A. (2012). Keepingthe world at hand: Rapid visuomotor processing forhandeobject interactions. Experimental Brain Research, 219(4),421e428. http://dx.doi.org/10.1007/s00221-012-3089-5.Makin, T. R., Holmes, N. P., & Zohary, E. (2007). Is that nearmy hand? Multisensory representation of peripersonalspace in human intraparietal sulcus. Journal of Neuroscience,27(4), 731e740. http://dx.doi.org/10.1523/JNEUROSCI.3653-06.2007.Makin, T. R., Wilf, M., Schwartz, I., & Zohary, E. (2010). Amputees“Neglect” the space near their missing hand. PsychologicalScience, 21(1), 55e57. http://dx.doi.org/10.1177/0956797609354739.Martel, M., Cardinali, L., Roy, A. C., & Farne, A. (2016). Tool-use: Anopen window into body representation and its plasticity.Cognitive Neuropsychology, 33(1e2), 82e101. http://dx.doi.org/10.1080/02643294.2016.1167678.Wandell, B. A., & Smirnakis, S. M. (2010). Plasticity and stability ofvisual field maps in adult primary visual cortex. Nature ReviewsNeuroscience, 10, 873e884. http://dx.doi.org/10.1038/nrn2741.

Peri-hand space representation in the absence of a hand - evidence from congenital one-handers

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