Abstract
Peripersonal space (PPS) is the space immediately surrounding the body, conceptualised as a sensory-motor interface between body and environment. PPS size differs between individuals and contexts, with intrapersonal traits and states, as well as social factors having a determining role on the size of PPS. Testosterone plays an important role in regulating social-motivational behaviour and is known to enhance dominance motivation in an implicit and unconscious manner. We investigated whether the dominance-enhancing effects of testosterone reflect as changes in the representation of PPS in a within-subjects testosterone administration study in women (N = 19). Participants performed a visuo-tactile integration task in a mixed-reality setup. Results indicated that the administration of testosterone caused a significant enlargement of participants’ PPS, suggesting that testosterone caused participants to implicitly appropriate a larger space as their own. These findings suggest that the dominance-enhancing effects of testosterone reflect at the level of sensory-motor processing in PPS.



Similar content being viewed by others
Code availability
Not applicable.
Availability of data and material
Not applicable.
References
Barrett FS, Robins RW, Janata P (2013) A brief form of the affective neuroscience personality scales. Psychol Assess 25(3):826
Bassolino M, Finisguerra A, Canzoneri E, Serino A, Pozzo T (2015) Dissociating effect of upper limb non-use and overuse on space and body representations. Neuropsychologia 70:385–392
Bausenhart KM, Di Luca M, Ulrich R (2018) Assessing duration discrimination: psychophysical methods and psychometric function analysis. In: Vatakis A, Balci F, Correa A, Di Luca M (eds) Timing and time perception: procedures, measures, and applications. Brill, pp 52–78. https://doi.org/10.1163/9789004280205_004
Bell MR, Sisk CL (2013) Dopamine mediates testosterone-induced social reward in male Syrian hamsters. Endocrinology 154(3):1225–1234
Bianchi VE (2019) The anti-inflammatory effects of testosterone. J Endocr Soc 3(1):91–107
Boksem MA, Mehta PH, Van den Bergh B, van Son V, Trautmann ST, Roelofs K, Sanfey AG (2013) Testosterone inhibits trust but promotes reciprocity. Psychol Sci 24(11):2306–2314
Bos PA, Terburg D, van Honk J (2010) Testosterone decreases trust in socially naïve humans. Proc Natl Acad Sci USA 107(22):9991–9995. https://doi.org/10.1073/pnas.0911700107
Bos PA, van Honk J, Ramsey NF, Stein DJ, Hermans EJ (2013) Testosterone administration in women increases amygdala responses to fearful and happy faces. Psychoneuroendocrinology 38(6):808–817
Brozzoli C, Cardinali L, Pavani F, Farnè A (2010) Action-specific remapping of peripersonal space. Neuropsychologia 48(3):796–802. https://doi.org/10.1016/j.neuropsychologia.2009.10.009
Canzoneri E, Ubaldi S, Rastelli V, Finisguerra A, Bassolino M, Serino A (2013) Tool-use reshapes the boundaries of body and peripersonal space representations. Exp Brain Res 228(1):25–42. https://doi.org/10.1007/s00221-013-3532-2
Carré JM, Archer J (2018) Testosterone and human behavior: the role of individual and contextual variables. Curr Opin Psychol 19:149–153
Casto KV, Edwards DA (2016) Testosterone, cortisol, and human competition. Horm Behav 82:21–37
Davis KL, Panksepp J (2011) The brain’s emotional foundations of human personality and the affective neuroscience personality scales. Neurosci Biobehav Rev 35(9):1946–1958
Davis KL, Panksepp J (2018) The emotional foundations of personality: a neurobiological and evolutionary approach. WW Norton & Company, New York
de Haan AM, Smit M, Van der Stigchel S, Dijkerman HC (2016) Approaching threat modulates visuotactile interactions in peripersonal space. Exp Brain Res 234(7):1875–1884
di Pellegrino G, Làdavas E (2015) Peripersonal space in the brain. Neuropsychologia 66:126–133. https://doi.org/10.1016/j.neuropsychologia.2014.11.011
Duhamel J-R, Colby CL, Goldberg ME (1998) Ventral intraparietal area of the macaque: congruent visual and somatic response properties. J Neurophysiol 79(1):126–136
Dunn BD, Stefanovitch I, Evans D, Oliver C, Hawkins A, Dalgleish T (2010) Can you feel the beat? Interoceptive awareness is an interactive function of anxiety-and depression-specific symptom dimensions. Behav Res Ther 48(11):1133–1138
Eisenegger C, Haushofer J, Fehr E (2011) The role of testosterone in social interaction. Trends Cogn Sci 15(6):263–271. https://doi.org/10.1016/j.tics.2011.04.008
Enter D, Spinhoven P, Roelofs K (2014) Alleviating social avoidance: effects of single dose testosterone administration on approach–avoidance action. Horm Behav 65(4):351–354. https://doi.org/10.1016/j.yhbeh.2014.02.001
Enter D, Terburg D, Harrewijn A, Spinhoven P, Roelofs K (2016) Single dose testosterone administration alleviates gaze avoidance in women with social anxiety disorder. Psychoneuroendocrinology 63:26–33. https://doi.org/10.1016/j.psyneuen.2015.09.008
Fogassi L, Gallese V, Fadiga L, Luppino G, Matelli M, Rizzolatti G (1996) Coding of peripersonal space in inferior premotor cortex (area F4). J Neurophysiol 76(1):141–157
Geir P, Selsbakk JM, Theresa W, Sigmund K (2014) Testing different versions of the affective neuroscience personality scales in a clinical sample. PLoS ONE 9(10):e109394
Graziano M, Cooke D (2006) Parieto–frontal interactions, personal space, and defensive behavior. Neuropsychologia 44(13):2621–2635. https://doi.org/10.1016/j.neuropsychologia.2005.09.009
Guterstam A, Szczotka J, Zeberg H, Ehrsson HH (2018) Tool use changes the spatial extension of the magnetic touch illusion. J Exp Psychol Gen 147(2):298
Hermans EJ, Putman P, Baas JM, Koppeschaar HP, van Honk J (2006a) A single administration of testosterone reduces fear-potentiated startle in humans. Biol Psychiatry 59(9):872–874. https://doi.org/10.1016/j.biopsych.2005.11.015
Hermans EJ, Putman P, van Honk J (2006b) Testosterone administration reduces empathetic behavior: a facial mimicry study. Psychoneuroendocrinology 31(7):859–866. https://doi.org/10.1016/j.psyneuen.2006.04.002
Hermans EJ, Putman P, Baas JM, Gecks NM, Kenemans JL, van Honk J (2007) Exogenous testosterone attenuates the integrated central stress response in healthy young women. Psychoneuroendocrinology 32(8–10):1052–1061
Hobeika L, Taffou M, Carpentier T, Warusfel O, Viaud-Delmon I (2020) Capturing the dynamics of peripersonal space by integrating expectancy effects and sound propagation properties. J Neurosci Methods 332:108534
Holmes NP, Martin D, Mitchell W, Noorani Z, Thorne A (2020) Do sounds near the hand facilitate tactile reaction times? Four experiments and a meta-analysis provide mixed support and suggest a small effect size. Exp Brain Res 1–15
Iachini T, Ruggiero G, Ruotolo F, di Cola AS, Senese VP (2015) The influence of anxiety and personality factors on comfort and reachability space: a correlational study. Cogn Process 16(1):255–258. https://doi.org/10.1007/s10339-015-0717-6
Iachini T, Coello Y, Frassinetti F, Senese VP, Galante F, Ruggiero G (2016) Peripersonal and interpersonal space in virtual and real environments: effects of gender and age. J Environ Psychol 45:154–164. https://doi.org/10.1016/j.jenvp.2016.01.004
Iriki A, Tanaka M, Iwamura Y (1996) Coding of modified body schema during tool use by macaque postcentral neurones. NeuroReport 7(14):2325–2330
Ishida H, Nakajima K, Inase M, Murata A (2010) Shared mapping of own and others’ bodies in visuotactile bimodal area of monkey parietal cortex. J Cogn Neurosci 22(1):83–96. https://doi.org/10.1162/jocn.2009.21185
Kandula M, Van der Stoep N, Hofman D, Dijkerman HC (2017) On the contribution of overt tactile expectations to visuo-tactile interactions within the peripersonal space. Exp Brain Res 235(8):2511–2522. https://doi.org/10.1007/s00221-017-4965-9
Maister L, Cardini F, Zamariola G, Serino A, Tsakiris M (2015) Your place or mine: shared sensory experiences elicit a remapping of peripersonal space. Neuropsychologia 70:455–461. https://doi.org/10.1016/j.neuropsychologia.2014.10.027
Makin TR, Holmes NP, Ehrsson HH (2008) On the other hand: dummy hands and peripersonal space. Behav Brain Res 191(1):1–10
Mazur A, Booth A (1998) Testosterone and dominance in men. Behav Brain Sci 21(3):353. https://doi.org/10.1017/S0140525X98001228
Miller J, Ulrich R (2001) On the analysis of psychometric functions: the Spearman–Kärber method. Percept Psychophys 63(8):1399–1420
Montoya ER, Terburg D, Bos PA, Will G-J, Buskens V, Raub W, van Honk J (2013) Testosterone administration modulates moral judgments depending on second-to-fourth digit ratio. Psychoneuroendocrinology 38(8):1362–1369
Moseley GL, Olthof N, Venema A, Don S, Wijers M, Gallace A, Spence C (2008) Psychologically induced cooling of a specific body part caused by the illusory ownership of an artificial counterpart. Proc Natl Acad Sci 105(35):13169–13173
Noel JP, Pfeiffer C, Blanke O, Serino A (2015a) Peripersonal space as the space of the bodily self. Cognition 144:49–57. https://doi.org/10.1016/j.cognition.2015.07.012
Noel J-P, Grivaz P, Marmaroli P, Lissek H, Blanke O, Serino A (2015b) Full body action remapping of peripersonal space: the case of walking. Neuropsychologia 70:375–384. https://doi.org/10.1016/j.neuropsychologia.2014.08.030
Noel J-P, Blanke O, Magosso E, Serino A (2018a) Neural adaptation accounts for the dynamic resizing of peripersonal space: evidence from a psychophysical–computational approach. J Neurophysiol 119(6):2307–2333. https://doi.org/10.1152/jn.00652.2017
Noel JP, Blanke O, Serino A (2018b) From multisensory integration in peripersonal space to bodily self-consciousness: from statistical regularities to statistical inference. Ann N Y Acad Sci 1426(1):146–165. https://doi.org/10.1111/nyas.13867
Noel J-P, Park H-D, Pasqualini I, Lissek H, Wallace M, Blanke O, Serino A (2018c) Audio-visual sensory deprivation degrades visuo-tactile peri-personal space. Conscious Cogn 61:61–75. https://doi.org/10.1016/j.concog.2018.04.001
Noel J-P, Samad M, Doxon A, Clark J, Keller S, Di Luca M (2018d) Peri-personal space as a prior in coupling visual and proprioceptive signals. Sci Rep 8(1):15819. https://doi.org/10.1038/s41598-018-33961-3
Noel J-P, Chatelle C, Perdikis S, Jöhr J, Da Silva ML, Ryvlin P, Serino A (2019) Peri-personal space encoding in patients with disorders of consciousness and cognitive-motor dissociation. Neuroimage Clin 24:101940
Noel J-P, Bertoni T, Terrebonne E, Pellencin E, Herbelin B, Cascio C, Serino A (2020) Rapid recalibration of peri-personal space: psychophysical, electrophysiological, and neural network modeling evidence. Cereb Cortex. https://doi.org/10.1093/cercor/bhaa103
Patané I, Cardinali L, Salemme R, Pavani F, Farnè A, Brozzoli C (2019) Action planning modulates peripersonal space. J Cogn Neurosci 31(8):1141–1154
Pellencin E, Paladino MP, Herbelin B, Serino A (2018) Social perception of others shapes one’s own multisensory peripersonal space. Cortex 104:163–179. https://doi.org/10.1016/j.cortex.2017.08.033
Pfeiffer C, Noel J-P, Serino A, Blanke O (2018) Vestibular modulation of peripersonal space boundaries. Eur J Neurosci 47(7):800–811. https://doi.org/10.1111/ejn.13872
Rizzolatti G, Scandolara C, Matelli M, Gentilucci M (1981a) Afferent properties of periarcuate neurons in macaque monkeys. I. Somatosensory responses. Behav Brain Res 2(2):125–146
Rizzolatti G, Scandolara C, Matelli M, Gentilucci M (1981b) Afferent properties of periarcuate neurons in macaque monkeys. II. Visual responses. Behav Brain Res 2(2):147–163
Salomon R, Noel J-P, Łukowska M, Faivre N, Metzinger T, Serino A, Blanke O (2017) Unconscious integration of multisensory bodily inputs in the peripersonal space shapes bodily self-consciousness. Cognition 166:174–183. https://doi.org/10.1016/j.cognition.2017.05.028
Sambo CF, Iannetti GD (2013) Better safe than sorry? the safety margin surrounding the body is increased by anxiety. J Neurosci 33(35):14225–14230. https://doi.org/10.1523/JNEUROSCI.0706-13.2013
Schutter DJ, Honk JV (2004) Decoupling of midfrontal delta–beta oscillations after testosterone administration. Int J Psychophysiol 53:71–73
Serino A (2019a) Peripersonal space (PPS) as a multisensory interface between the individual and the environment, defining the space of the self. Neurosci Biobehav Rev. https://doi.org/10.1016/j.neubiorev.2019.01.016
Serino A (2019b) Peripersonal space (PPS) as a multisensory interface between the individual and the environment, defining the space of the self. Neurosci Biobehav Rev 99:138–159
Serino A, Bassolino M, Farnè A, Làdavas E (2007) Extended multisensory space in blind cane users. Psychol Sci 18(7):642–648. https://doi.org/10.1111/j.1467-9280.2007.01952.x
Serino A, Canzoneri E, Marzolla M, di Pellegrino G, Magosso E (2015a) Extending peripersonal space representation without tool-use: evidence from a combined behavioral-computational approach. Front Behav Neurosci. https://doi.org/10.3389/fnbeh.2015.00004
Serino A, Noel JP, Galli G, Canzoneri E, Marmaroli P, Lissek H, Blanke O (2015b) Body part-centered and full body-centered peripersonal space representations. Sci Rep 5:18603. https://doi.org/10.1038/srep18603
Serino A, Noel JP, Mange R, Canzoneri E, Pellencin E, Ruiz JB, Herbelin B (2018) Peripersonal space: an index of multisensory body-environment interactions in real, virtual, and mixed realities. Front ICT 4:31. https://doi.org/10.3389/fict.2017.00031
Sinervo B, Miles DB, Frankino WA, Klukowski M, DeNardo DF (2000) Testosterone, endurance, and Darwinian fitness: natural and sexual selection on the physiological bases of alternative male behaviors in side-blotched lizards. Horm Behav 38(4):222–233
Sinnesael M, Boonen S, Claessens F, Gielen E, Vanderschueren D (2011) Testosterone and the male skeleton: a dual mode of action. J Osteoporos 2011:240328. https://doi.org/10.4061/2011/240328
Spaccasassi C, Maravita A (2020) Peripersonal space is diversely sensitive to a temporary vs permanent state of anxiety. Cognition 195:104133
Spielberger CD, Gorsuch RL, Lushene RE (1970) Manual for the state-trait anxiety inventory. Consulting Psychologists Press, Palo Alto
Stanton SJ, Schultheiss OC (2009) The hormonal correlates of implicit power motivation. J Res Pers 43(5):942–949. https://doi.org/10.1016/j.jrp.2009.04.001
Stone KD, Kandula M, Keizer A, Dijkerman HC (2018) Peripersonal space boundaries around the lower limbs. Exp Brain Res 236(1):161–173
Taffou M, Viaud-Delmon I (2014) Cynophobic fear adaptively extends peri-personal space. Front Psychiatry 5:122. https://doi.org/10.3389/fpsyt.2014.00122
Teneggi C, Canzoneri E, di Pellegrino G, Serino A (2013) Social modulation of peripersonal space boundaries. Curr Biol 23(5):406–411. https://doi.org/10.1016/j.cub.2013.01.043
Teramoto W (2018) A behavioral approach to shared mapping of peripersonal space between oneself and others. Sci Rep 8(1):5432. https://doi.org/10.1038/s41598-018-23815-3
Terburg D, van Honk J (2013) Approach–avoidance versus dominance–submissiveness: a multilevel neural framework on how testosterone promotes social status. Emot Rev 5(3):296–302. https://doi.org/10.1177/1754073913477510
Terburg D, Aarts H, van Honk J (2012) Testosterone affects gaze aversion from angry faces outside of conscious awareness. Psychol Sci (0956-7976) 23(5):459–463. https://doi.org/10.1177/0956797611433336
Terburg D, Syal S, Rosenberger LA, Heany SJ, Stein DJ, Honk J, v. (2016) Testosterone abolishes implicit subordination in social anxiety. Psychoneuroendocrinology 72:205–211. https://doi.org/10.1016/j.psyneuen.2016.07.203
Tuiten A, Van Honk J, Koppeschaar H, Bernaards C, Thijssen J, Verbaten R (2000) Time course of effects of testosterone administration on sexual arousal in women. Arch Gen Psychiatry 57(2):149–153. https://doi.org/10.1001/archpsyc.57.2.149
van der Westhuizen D, Solms M (2015) Social dominance and the affective neuroscience personality scales. Conscious Cogn 33:90–111. https://doi.org/10.1016/j.concog.2014.12.005
van der Westhuizen D, Moore J, Solms M, van Honk J (2017) Testosterone facilitates the sense of agency. Conscious Cogn 56:58–67. https://doi.org/10.1016/j.concog.2017.10.005
van der Westhuizen D, Page T, Solms M, van Honk J (2019) The territory of my body: testosterone prevents limb cooling in the rubber hand illusion. Multisens Res 1(aop):1–27
van Honk J, Tuiten A (2001) A single administration of testosterone induces cardiac accelerative responses to angry faces in healthy young women. Behav Neurosci 115(1):238. https://doi.org/10.1037/0735-7044.115.1.238
van Honk J, Tuiten A, Verbaten R, van den Hout M, Koppeschaar H, Thijssen J, de Haan E (1999) Correlations among salivary testosterone, mood, and selective attention to threat in humans. Horm Behav 36(1):17–24. https://doi.org/10.1006/hbeh.1999.1521
van Honk J, Peper JS, Schutter DJLG (2005) Testosterone reduces unconscious fear but not consciously experienced anxiety: implications for the disorders of fear and anxiety. Biol Psychiatry 58(3):218–225. https://doi.org/10.1016/j.biopsych.2005.04.003
van Honk J, Schutter DJLG (2007) Testosterone reduces conscious detection of signals serving social correction: implications for antisocial behavior. Psychol Sci 18(8):663–667. https://doi.org/10.1111/j.1467-9280.2007.01955.x
van Honk J, Schutter DJ, Bos PA, Kruijt A-W, Lentjes EG, Baron-Cohen S (2011) Testosterone administration impairs cognitive empathy in women depending on second-to-fourth digit ratio. Proc Natl Acad Sci. https://doi.org/10.1073/pnas.1011891108
Vergallito A, Gerfo EL, Varoli E, Brambilla M, Sacchi S, Anzani S, Lauro LR (2019) Positive self-perception and corticospinal excitability: recalling positive behavior expands peripersonal space boundaries. Neuropsychologia 135:107224
Wagels L, Radke S, Goerlich KS, Habel U, Votinov M (2017) Exogenous testosterone decreases men’s personal distance in a social threat context. Horm Behav 90:75–83. https://doi.org/10.1016/j.yhbeh.2017.03.001
Wang C, Swerdloff RS, Iranmanesh A, Dobs A, Snyder PJ, Cunningham G, Testosterone Gel Study Group, N (2000) Transdermal testosterone gel improves sexual function, mood, muscle strength, and body composition parameters in hypogonadal men. J Clin Endocrinol Metab 85(8):2839–2853
Wirth MM, Schultheiss OC (2007) Basal testosterone moderates responses to anger faces in humans. Physiol Behav 90(2):496–505. https://doi.org/10.1016/j.physbeh.2006.10.016
Wright ND, Bahrami B, Johnson E, Malta GD, Rees G, Frith CD, Dolan RJ (2012) Testosterone disrupts human collaboration by increasing egocentric choices. Proc R Soc B Biol Sci 279(1736):2275–2280. https://doi.org/10.1098/rspb.2011.2523
Funding
CJM received support from the University of Cape Town and the Ernst & Ethel Erickson Trust.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
On behalf of all authors, the corresponding author states that there is no conflict of interest.
Ethics approval
This research involved human participants. The study was approved by the local ethics committees—the University of Cape Town (UCT) Psychology Department and the UCT Health Sciences Human Research Ethics Committee. The study was performed in accordance with the ethical standards laid down in the 1964 Declaration of Helsinki.
Consent to participate
All participants gave informed written consent to take part in the study.
Additional information
Communicated by Francesca Frassinetti.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Masson, C., van der Westhuizen, D., Noel, JP. et al. Testosterone administration in women increases the size of their peripersonal space. Exp Brain Res 239, 1639–1649 (2021). https://doi.org/10.1007/s00221-021-06080-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00221-021-06080-1