Spatial reference frames (RFs) play a key role in spatial cognition, especially in perception, spatial memory, and navigation. There are two main types of RFs: egocentric (self-centered) and allocentric (object-centered). Although many fMRI studies examined the neural correlates of egocentric and allocentric RFs, they could not sample the fast temporal dynamics of the underlying cognitive processes. Therefore, the interaction and timing between these two RFs remain unclear. Taking advantage of the high temporal resolution of intracranial EEG (iEEG), we aimed to determine the timing of egocentric and allocentric information processing and describe the brain areas involved. We recorded iEEG and analyzed broad gamma activity (50-150 Hz) in 37 epilepsy patients performing a spatial judgment task in a three-dimensional circular virtual arena. We found overlapping activation for egocentric and allocentric RFs in many brain regions, with several additional egocentric- and allocentric-selective areas. In contrast to the egocentric responses, the allocentric responses peaked later than the control ones in frontal regions with overlapping selectivity. Also, across several egocentric or allocentric selective areas, the egocentric selectivity appeared earlier than the allocentric one. We identified the maximum number of egocentric-selective channels in the medial occipito-temporal region and allocentric-selective channels around the intraparietal sulcus in the parietal cortex. Our findings favor the hypothesis that egocentric spatial coding is a more primary process, and allocentric representations may be derived from egocentric ones. They also broaden the dominant view of the dorsal and ventral streams supporting egocentric and allocentric space coding, respectively.

3rd Faculty of Medicine Charles University Prague Czechia

Department of Circuit Theory Faculty of Electrical Engineering Czech Technical University Prague Prague Czechia

Department of Neurology 2nd Faculty of Medicine Charles University and Motol University Hospital Prague Czechia

Laboratory of Neurophysiology of Memory Institute of Physiology Czech Academy of Sciences Videnska 1083 142 20 Prague Czechia

Zobrazit více v PubMed

Abdi H, Williams LJ, United States (2010) Tukey’s honestly significant difference (HSD) test. N. Salkind (Ed.), Encyclopedia of research design: Qualitative research, SAGE Publications, Inc, (2010), pp. 1159–1164, 10.4135/9781412961288

Bastin J, Committeri G, Kahane P, Galati G, Minotti L, Lachaux JP, Berthoz A. Timing of posterior parahippocampal gyrus activity reveals multiple scene processing stages. Hum Brain Mapp. 2013;34(6):1357–1370. doi: 10.1002/hbm.21515. PubMed DOI PMC

Byrne P, Becker S, Burgess N. Remembering the past and imagining the future: a neural model of spatial memory and imagery. Psychol Rev. 2007;114(2):340–375. doi: 10.1037/0033-295X.114.2.340. PubMed DOI PMC

Chechlacz M, Rotshtein P, Bickerton WL, Hansen PC, Deb S, Humphreys GW. Separating neural correlates of allocentric and egocentric neglect: distinct cortical sites and common white matter disconnections. Cogn Neuropsychol. 2010;27(3):277–303. doi: 10.1080/02643294.2010.519699. PubMed DOI

Chechlacz M, Rotshtein P, Humphreys GW. Neuroanatomical dissections of unilateral visual neglect symptoms: ALE Meta-analysis of lesion-symptom mapping. Front Hum Neurosci. 2012;6:230. doi: 10.3389/fnhum.2012.00230. PubMed DOI PMC

Committeri G, Galati G, Paradis AL, Pizzamiglio L, Berthoz A, LeBihan D. Reference frames for spatial cognition: different brain areas are involved in viewer-, object-, and landmark-centered judgments about object location. J Cogn Neurosci. 2004;16(9):1517–1535. doi: 10.1162/0898929042568550. PubMed DOI

Corbetta M, Shulman GL. Control of goal-directed and stimulus-driven attention in the brain. Nat Rev Neurosci. 2002;3(3):201–215. doi: 10.1038/nrn755. PubMed DOI

Dempsey LA, Cooper RJ, Roque T, Correia T, Magee E, Powell S, Hebden JC. Data-driven approach to optimum wavelength selection for diffuse optical imaging. J Biomed Opt. 2015;20(1):016003. doi: 10.1117/1.JBO.20.1.016003. PubMed DOI

Derbie AY, Chau BKH, Wong CHY, Chen LD, Ting KH, Lam BYH, Chan CCH. Common and distinct neural trends of allocentric and egocentric spatial coding: an ALE Meta-analysis. Eur J Neurosci. 2021 doi: 10.1111/ejn.15240. PubMed DOI

Derbie AY, Chau B, Lam B, Fang YH, Ting KH, Wong CY, Chan H. Cortical hemodynamic response Associated with spatial coding: a Near-Infrared Spectroscopy Study. Brain Topogr. 2021;34(2):207–220. doi: 10.1007/s10548-021-00821-9. PubMed DOI

Dilks DD, Julian JB, Paunov AM, Kanwisher N. The occipital place area is causally and selectively involved in scene perception. J Neurosci. 2013;33(4):1331–1336a. doi: 10.1523/JNEUROSCI.4081-12.2013. PubMed DOI PMC

Fajnerova I, Rodriguez M, Levcik D, Konradova L, Mikolas P, Brom C, Horacek J. A virtual reality task based on animal research - spatial learning and memory in patients after the first episode of schizophrenia. Front Behav Neurosci. 2014;8:157. doi: 10.3389/fnbeh.2014.00157. PubMed DOI PMC

Filimon F. Are all spatial reference frames egocentric? Reinterpreting evidence for Allocentric, Object-Centered, or World-Centered reference frames. Front Hum Neurosci. 2015;9:648. doi: 10.3389/fnhum.2015.00648. PubMed DOI PMC

Galati G, Lobel E, Vallar G, Berthoz A, Pizzamiglio L, Le Bihan D. The neural basis of egocentric and allocentric coding of space in humans: a functional magnetic resonance study. Exp Brain Res. 2000;133(2):156–164. doi: 10.1007/s002210000375. PubMed DOI

Galati G, Pelle G, Berthoz A, Committeri G. Multiple reference frames used by the human brain for spatial perception and memory. Exp Brain Res. 2010;206(2):109–120. doi: 10.1007/s00221-010-2168-8. PubMed DOI

Genovese CR, Lazar NA, Nichols T. Thresholding of statistical maps in functional neuroimaging using the false discovery rate. NeuroImage. 2002;15(4):870–878. doi: 10.1006/nimg.2001.1037. PubMed DOI

Gomez A, Rousset S, Charnallet A. Spatial deficits in an amnesic patient with hippocampal damage: questioning the multiple trace theory. Hippocampus. 2012;22(6):1313–1324. doi: 10.1002/hipo.20968. PubMed DOI

Gomez A, Cerles M, Rousset S, Remy C, Baciu M. Differential hippocampal and retrosplenial involvement in egocentric-updating, rotation, and allocentric processing during online spatial encoding: an fMRI study. Front Hum Neurosci. 2014;8:150. doi: 10.3389/fnhum.2014.00150. PubMed DOI PMC

Goodale MA, Milner AD. Separate visual pathways for perception and action. Trends Neurosci. 1992;15(1):20–25. doi: 10.1016/0166-2236(92)90344-8. PubMed DOI

Goodale MA, Westwood DA, Milner AD (2004) Two distinct modes of control for object-directed action. In: The roots of visual awareness: a festschrift in honour of Alan Cowey, pp 131–144. 10.1016/s0079-6123(03)14409-3 PubMed

Grefkes C, Fink GR. The functional organization of the intraparietal sulcus in humans and monkeys. J Anat. 2005;207(1):3–17. doi: 10.1111/j.1469-7580.2005.00426.x. PubMed DOI PMC

Grimsen C, Hildebrandt H, Fahle M. Dissociation of egocentric and allocentric coding of space in visual search after right middle cerebral artery stroke. Neuropsychologia. 2008;46(3):902–914. doi: 10.1016/j.neuropsychologia.2007.11.028. PubMed DOI

Hammer J, Pistohl T, Fischer J, Krsek P, Tomasek M, Marusic P, Ball T. Predominance of Movement Speed over direction in neuronal Population signals of Motor Cortex: intracranial EEG data and a simple explanatory model. Cereb Cortex. 2016;26(6):2863–2881. doi: 10.1093/cercor/bhw033. PubMed DOI PMC

Hirshhorn M, Grady C, Rosenbaum RS, Winocur G, Moscovitch M. The hippocampus is involved in mental navigation for a recently learned, but not a highly familiar environment: a longitudinal fMRI study. Hippocampus. 2012;22(4):842–852. doi: 10.1002/hipo.20944. PubMed DOI

Hutchison RM, Gallivan JP. Functional coupling between frontoparietal and occipitotemporal pathways during action and perception. Cortex. 2018;98:8–27. doi: 10.1016/j.cortex.2016.10.020. PubMed DOI

Iaria G, Chen JK, Guariglia C, Ptito A, Petrides M. Retrosplenial and hippocampal brain regions in human navigation: complementary functional contributions to the formation and use of cognitive maps. Eur J Neurosci. 2007;25(3):890–899. doi: 10.1111/j.1460-9568.2007.05371.x. PubMed DOI

Janca R, Jezdik P, Cmejla R, Tomasek M, Worrell GA, Stead M, Marusic P. Detection of interictal epileptiform discharges using signal envelope distribution modelling: application to epileptic and non-epileptic intracranial recordings. Brain Topogr. 2015;28(1):172–183. doi: 10.1007/s10548-014-0379-1. PubMed DOI

Janzen G, van Turennout M. Selective neural representation of objects relevant for navigation. Nat Neurosci. 2004;7(6):673–677. doi: 10.1038/nn1257. PubMed DOI

Jordan K, Schadow J, Wuestenberg T, Heinze HJ, Jancke L. Different cortical activations for subjects using allocentric or egocentric strategies in a virtual navigation task. NeuroReport. 2004;15(1):135–140. doi: 10.1097/00001756-200401190-00026. PubMed DOI

Julian JB, Ryan J, Hamilton RH, Epstein RA. The Occipital Place Area is causally involved in representing environmental boundaries during Navigation. Curr Biol. 2016;26(8):1104–1109. doi: 10.1016/j.cub.2016.02.066. PubMed DOI PMC

Kamps FS, Julian JB, Kubilius J, Kanwisher N, Dilks DD. The occipital place area represents the local elements of scenes. NeuroImage. 2016;132:417–424. doi: 10.1016/j.neuroimage.2016.02.062. PubMed DOI PMC

Klatzky RL. Allocentric and egocentric spatial representations: definitions, distinctions, and interconnections. In: Freksa C, Habel C, Wender KF, editors. Spatial cognition: an Interdisciplinary Approach to representing and Processing spatial knowledge. Berlin Heidelberg: Springer; 1998. pp. 1–17.

Kravitz DJ, Saleem KS, Baker CI, Mishkin M. A new neural framework for visuospatial processing. Nat Rev Neurosci. 2011;12(4):217–230. doi: 10.1038/nrn3008. PubMed DOI PMC

Kunz L, Brandt A, Reinacher PC, Staresina BP, Reifenstein ET, Weidemann CT, Jacobs J. A neural code for egocentric spatial maps in the human medial temporal lobe. Neuron. 2021 doi: 10.1016/j.neuron.2021.06.019. PubMed DOI PMC

Lachaux JP, Axmacher N, Mormann F, Halgren E, Crone NE. High-frequency neural activity and human cognition: past, present and possible future of intracranial EEG research. Prog Neurobiol. 2012;98(3):279–301. doi: 10.1016/j.pneurobio.2012.06.008. PubMed DOI PMC

Li J, Zhang R, Liu S, Liang Q, Zheng S, He X, Huang R. Human spatial navigation: neural representations of spatial scales and reference frames obtained from an ALE meta-analysis. NeuroImage. 2021;238:118264. doi: 10.1016/j.neuroimage.2021.118264. PubMed DOI

Lifshitz M, Thibault RT, Roth RR, Raz A. Source localization of Brain States Associated with Canonical Neuroimaging Postures. J Cogn Neurosci. 2017;29(7):1292–1301. doi: 10.1162/jocn_a_01107. PubMed DOI

Maguire EA, Burgess N, Donnett JG, Frackowiak RS, Frith CD, O’Keefe J. Knowing where and getting there: a human navigation network. Science. 1998;280(5365):921–924. doi: 10.1126/science.280.5365.921. PubMed DOI

Mai JK, Majtanik M, Paxinos G (2015) Atlas of the human brain. Academic Press

Manning JR, Jacobs J, Fried I, Kahana MJ. Broadband shifts in local field potential power spectra are correlated with single-neuron spiking in humans. J Neurosci. 2009;29(43):13613–13620. doi: 10.1523/JNEUROSCI.2041-09.2009. PubMed DOI PMC

Miller KJ, Honey CJ, Hermes D, Rao RP, denNijs M, Ojemann JG. Broadband changes in the cortical surface potential track activation of functionally diverse neuronal populations. Neuroimage 85 Pt. 2014;2:711–720. doi: 10.1016/j.neuroimage.2013.08.070. PubMed DOI PMC

Miyakoshi M, Gehrke L, Gramann K, Makeig S, Iversen J. The AudioMaze: an EEG and motion capture study of human spatial navigation in sparse augmented reality. Eur J Neurosci. 2021 doi: 10.1111/ejn.15131. PubMed DOI

Moraresku S, Vlcek K. The use of egocentric and allocentric reference frames in static and dynamic conditions in humans. Physiol Res. 2020;69(5):787–801. doi: 10.33549/physiolres.934528. PubMed DOI PMC

Mukamel R, Gelbard H, Arieli A, Hasson U, Fried I, Malach R. Coupling between neuronal firing, field potentials, and FMRI in human auditory cortex. Science. 2005;309(5736):951–954. doi: 10.1126/science.1110913. PubMed DOI

Musch K, Hamame CM, Perrone-Bertolotti M, Minotti L, Kahane P, Engel AK, Schneider TR. Selective attention modulates high-frequency activity in the face-processing network. Cortex. 2014;60:34–51. doi: 10.1016/j.cortex.2014.06.006. PubMed DOI

Nakamura K, Kawashima R, Sato N, Nakamura A, Sugiura M, Kato T, Zilles K (2000) Functional delineation of the human occipito-temporal areas related to face and scene processing. A PET study. Brain 123 (Pt 91903–1912. 10.1093/brain/123.9.1903 PubMed

Nyffeler T, Gutbrod K, Pflugshaupt T, Vonwartburg R, Hess C, Muri R. Allocentric and egocentric spatial impairments in a case of Topographical Disorientation. Cortex. 2005;41(2):133–143. doi: 10.1016/s0010-9452(08)70888-8. PubMed DOI

Ojemann GA, Corina DP, Corrigan N, Schoenfield-McNeill J, Poliakov A, Zamora L, Zanos S (2010) Neuronal correlates of functional magnetic resonance imaging in human temporal cortex. Brain 133 Pt 146–59. 10.1093/brain/awp227 PubMed PMC

Parslow DM, Rose D, Brooks B, Fleminger S, Gray JA, Giampietro V, Morris RG. Allocentric spatial memory activation of the hippocampal formation measured with fMRI. Neuropsychology. 2004;18(3):450–461. doi: 10.1037/0894-4105.18.3.450. PubMed DOI

Peirce J, Gray JR, Simpson S, MacAskill M, Hochenberger R, Sogo H, Lindelov JK. PsychoPy2: experiments in behavior made easy. Behav Res Methods. 2019;51(1):195–203. doi: 10.3758/s13428-018-01193-y. PubMed DOI PMC

Ptak R. The frontoparietal attention network of the human brain: action, saliency, and a priority map of the environment. Neuroscientist. 2012;18(5):502–515. doi: 10.1177/1073858411409051. PubMed DOI

Ray D, Hajare N, Roy D, Banerjee A (2020) Large-scale functional integration, rather than functional dissociation along dorsal and ventral streams, underlies visual perception and action. J Cogn Neurosci 32(5):847–861. 10.1162/jocn_a_01527 PubMed

Rodriguez PF. Human navigation that requires calculating heading vectors recruits parietal cortex in a virtual and visually sparse water maze task in fMRI. Behav Neurosci. 2010;124(4):532–540. doi: 10.1037/a0020231. PubMed DOI

Rosenbaum RS, Ziegler M, Winocur G, Grady CL, Moscovitch M. I have often walked down this street before”: fMRI studies on the hippocampus and other structures during mental navigation of an old environment. Hippocampus. 2004;14(7):826–835. doi: 10.1002/hipo.10218. PubMed DOI

Ruggiero G, Iachini T, Ruotolo F, Senese V (2009) Spatial Memory: the role of egocentric and allocentric frames of reference In Thomas JB (Ed.), Spatial Memory: Visuospatial processes, cognitive performance and developmental effects (pp. 51–75). Hauppauge, NY: Nova Science Publishers

Ruggiero G, D’Errico O, Iachini T. Development of egocentric and allocentric spatial representations from childhood to elderly age. Psychol Res. 2016;80(2):259–272. doi: 10.1007/s00426-015-0658-9. PubMed DOI

Ruotolo F, Ruggiero G, Raemaekers M, Iachini T, van der Ham IJM, Fracasso A, Postma A. Neural correlates of egocentric and allocentric frames of reference combined with metric and non-metric spatial relations. Neuroscience. 2019;409:235–252. doi: 10.1016/j.neuroscience.2019.04.021. PubMed DOI

Saj A, Cojan Y, Musel B, Honore J, Borel L, Vuilleumier P. Functional neuro-anatomy of egocentric versus allocentric space representation. Neurophysiol Clin. 2014;44(1):33–40. doi: 10.1016/j.neucli.2013.10.135. PubMed DOI

Sato N, Nakamura K, Nakamura A, Sugiura M, Ito K, Fukuda H, Kawashima R. Different time course between scene processing and face processing: a MEG study. NeuroReport. 1999;10(17):3633–3637. doi: 10.1097/00001756-199911260-00031. PubMed DOI

Spiers HJ, Maguire EA. A navigational guidance system in the human brain. Hippocampus. 2007;17(8):618–626. doi: 10.1002/hipo.20298. PubMed DOI PMC

Szczepanski SM, Konen CS, Kastner S. Mechanisms of spatial attention control in frontal and parietal cortex. J Neurosci. 2010;30(1):148–160. doi: 10.1523/JNEUROSCI.3862-09.2010. PubMed DOI PMC

Tanji J, Hoshi E. Role of the lateral prefrontal cortex in executive behavioral control. Physiol Rev. 2008;88(1):37–57. doi: 10.1152/physrev.00014.2007. PubMed DOI

Tsutsui K, Taira M, Sakata H. Neural mechanisms of three-dimensional vision. Neurosci Res. 2005;51(3):221–229. doi: 10.1016/j.neures.2004.11.006. PubMed DOI

Vidal JR, Ossandon T, Jerbi K, Dalal SS, Minotti L, Ryvlin P, Lachaux JP. Category-specific visual responses: an intracranial study comparing Gamma, Beta, Alpha, and ERP Response selectivity. Front Hum Neurosci. 2010;4:195. doi: 10.3389/fnhum.2010.00195. PubMed DOI PMC

Vlcek K, Fajnerova I, Nekovarova T, Hejtmanek L, Janca R, Jezdik P, Marusic P. Mapping the scene and object Processing Networks by Intracranial EEG. Front Hum Neurosci. 2020;14:561399. doi: 10.3389/fnhum.2020.561399. PubMed DOI PMC

Weniger G, Irle E. Posterior parahippocampal gyrus lesions in the human impair egocentric learning in a virtual environment. Eur J Neurosci. 2006;24(8):2406–2414. doi: 10.1111/j.1460-9568.2006.05108.x. PubMed DOI

Weniger G, Siemerkus J, Schmidt-Samoa C, Mehlitz M, Baudewig J, Dechent P, Irle E. The human parahippocampal cortex subserves egocentric spatial learning during navigation in a virtual maze. Neurobiol Learn Mem. 2010;93(1):46–55. doi: 10.1016/j.nlm.2009.08.003. PubMed DOI

Wilson KD, Woldorff MG, Mangun GR. Control networks and hemispheric asymmetries in parietal cortex during attentional orienting in different spatial reference frames. NeuroImage. 2005;25(3):668–683. doi: 10.1016/j.neuroimage.2004.07.075. PubMed DOI

Zaehle T, Jordan K, Wustenberg T, Baudewig J, Dechent P, Mast FW. The neural basis of the egocentric and allocentric spatial frame of reference. Brain Res. 2007;1137(1):92–103. doi: 10.1016/j.brainres.2006.12.044. PubMed DOI

Antagonistic behavior of brain networks mediated by low-frequency oscillations: electrophysiological dynamics during internal-external attention switching