Abstract
The retrosplenial complex is a region within the posterior cingulate cortex implicated in spatial navigation. Here, we investigated the functional specialization of this large and anatomically heterogeneous region using fMRI and resting-state functional connectivity combined with a spatial task with distinct phases of spatial ‘updating’ (i.e., integrating and maintaining object locations in memory during spatial displacement) and ‘orienting’ (i.e., recalling unseen locations from current position in space). Both spatial ‘updating’ and ‘orienting’ produced bilateral activity in the retrosplenial complex, among other areas. However, spatial ‘updating’ produced slightly greater activity in ventro-lateral portions, of the retrosplenial complex, whereas spatial ‘orienting’ produced greater activity in a more dorsal and medial portion of it (both regions localized along the parieto-occipital fissure). At rest, both ventro-lateral and dorso-medial subregions of the retrosplenial complex were functionally connected to the hippocampus and parahippocampus, regions both involved in spatial orientation and navigation. However, the ventro-lateral subregion of the retrosplenial complex displayed more positive functional connectivity with ventral occipital and temporal object recognition regions, whereas the dorso-medial subregion activity was more correlated to dorsal activity and frontal activity, as well as negatively correlated with more ventral parietal structures. These findings provide evidence for a dorso-medial to ventro-lateral functional specialization within the human retrosplenial complex that may shed more light on the complex neural mechanisms underlying spatial orientation and navigation in humans.
Similar content being viewed by others
References
Aggleton JP, Saunders RC, Wright NF, Vann SD (2014) The origin of projections from the posterior cingulate and retrosplenial cortices to the anterior, medial dorsal and laterodorsal thalamic nuclei of macaque monkeys. Eur J Neurosci 39:107–123. doi:10.1111/ejn.12389
Aguirre GK, D’Esposito M (1999) Topographical disorientation: a synthesis and taxonomy. Brain 122:1613–1628. doi:10.1093/brain/122.9.1613
Auger SD, Maguire EA (2013) Assessing the mechanism of response in the retrosplenial cortex of good and poor navigators. Cortex 49:2904–2913. doi:10.1016/j.cortex.2013.08.002
Bahlmann J, Schubotz RI, Mueller JL et al (2009) Neural circuits of hierarchical visuo-spatial sequence processing. Brain Res 1298:161–170. doi:10.1016/j.brainres.2009.08.017
Baldassano C, Beck DM, Fei-Fei L (2013) Differential connectivity within the Parahippocampal Place Area. Neuroimage 75:228–237. doi:10.1016/j.neuroimage.2013.02.073
Beckmann M, Johansen-Berg H, Rushworth MFS (2009) Connectivity-based parcellation of human cingulate cortex and its relation to functional specialization. J Neurosci 29:1175–1190. doi:10.1523/JNEUROSCI.3328-08.2009
Binder JR, Frost JA, Hammeke TA et al (1997) Human brain language areas identified by functional magnetic resonance imaging. J Neurosci 17:353–362
Bowers D, Verfaellie M, Valenstein E, Heilman KM (1988) Impaired acquisition of temporal information in retrosplenial amnesia. Brain Cogn 8:47–66. doi:10.1016/0278-2626(88)90038-3
Brodmann K (2006) Brodmann’s Localisation in the cerebral cortex the principles of comparative localisation in the cerebral cortex based on cytoarchitectonics, 3rd edn. Springer, New York
Burgess N, Becker S, King JA, O’Keefe J (2001) Memory for events and their spatial context: models and experiments. Philos Trans R Soc Lond B Biol Sci 356:1493–1503. doi:10.1098/rstb.2001.0948
Cavanna AE, Trimble MR (2006) The precuneus: a review of its functional anatomy and behavioural correlates. Brain 129:564–583. doi:10.1093/brain/awl004
Chadwick MJ, Spiers HJ (2014) A local anchor for the brain’s compass. Nat Neurosci 17:1436–1437. doi:10.1038/nn.3841
Cho J, Sharp PE (2001) Head Direction, Place, and Movement Correlates for Cells in the Rat Retrosplenial Cortex. Behav Neurosci 115:3–25. doi:10.1037/0735-7044.115.1.3
de Fockert JW (2001) The role of working memory in visual selective attention. Science 291:1803–1806. doi:10.1126/science.1056496
Epstein RA (2008) Parahippocampal and retrosplenial contributions to human spatial navigation. Trends Cogn Sci 12:388–396. doi:10.1016/j.tics.2008.07.004
Fox MD, Snyder AZ, Vincent JL et al (2005) The human brain is intrinsically organized into dynamic, anticorrelated functional networks. Proc Natl Acad Sci USA 102:9673–9678. doi:10.1073/pnas.0504136102
Iaria G, Chen J-K, Guariglia C et al (2007) Retrosplenial and hippocampal brain regions in human navigation: complementary functional contributions to the formation and use of cognitive maps. Eur J Neurosci 25:890–899. doi:10.1111/j.1460-9568.2007.05371.x
Ino T, Inoue Y, Kage M et al (2002) Mental navigation in humans is processed in the anterior bank of the parieto-occipital sulcus. Neurosci Lett 322:182–186. doi:10.1016/S0304-3940(02)00019-8
Ino T, Doi T, Hirose T et al (2007) Directional disorientation following left retrosplenial hemorrhage: a case report with fMRI studies. Cortex 43:248–254. doi:10.1016/S0010-9452(08)70479-9
Karnath HO, Berger MF, Küker W, Rorden C (2004) The anatomy of spatial neglect based on voxelwise statistical analysis: a study of 140 patients. Cereb Cortex 14:1164–1172. doi:10.1093/cercor/bhh076
Koechlin E, Jubault T (2006) Broca’s Area and the Hierarchical Organization of Human Behavior. Neuron 50:963–974. doi:10.1016/j.neuron.2006.05.017
Leech R, Braga R, Sharp DJ (2012) Echoes of the brain within the posterior cingulate cortex. J Neurosci 32:215–222. doi:10.1523/JNEUROSCI.3689-11.2012
Machielsen WCM, Rombouts SARB, Barkhof F et al (2000) fMRI of visual encoding: reproducibility of activation. Hum Brain Mapp 9:156–164. doi:10.1002/(SICI)1097-0193(200003)9:3<156:AID-HBM4>3.0.CO;2-Q
Maddock RJ (1999) The retrosplenial cortex and emotion: new insights from functional neuroimaging of the human brain. Trends Neurosci 22:310–316. doi:10.1016/S0166-2236(98)01374-5
Maddock RJ, Garrett AS, Buonocore MH (2001) Remembering familiar people: the posterior cingulate cortex and autobiographical memory retrieval. Neuroscience 104:667–676. doi:10.1016/S0306-4522(01)00108-7
Maguire EA (2001) The retrosplenial contribution to human navigation: a review of lesion and neuroimaging findings. Scand J Psychol 42:225–238. doi:10.1111/1467-9450.00233
Maguire EA, Frith CD, Burgess N et al (1998) Knowing where things are: parahippocampal involvement in encoding object locations in virtual large-scale space. J Cogn Neurosci 10:61–76. doi:10.1162/089892998563789
Maguire EA, Gadian DG, Johnsrude IS et al (2000) Navigation-related structural change in the hippocampi of taxi drivers. Proc Natl Acad Sci USA 97:4398–4403. doi:10.1073/pnas.070039597
Maguire EA, Woollett K, Spiers HJ (2006) London taxi drivers and bus drivers: a structural MRI and neuropsychological analysis. Hippocampus 16:1091–1101. doi:10.1002/hipo
Marchette SA, Vass LK, Ryan J, Epstein RA (2014) Anchoring the neural compass: coding of local spatial reference frames in human medial parietal lobe. Nat Neurosci 17:1598–1606. doi:10.1038/nn.3834
Margulies DS, Vincent JL, Kelly C et al (2009) Precuneus shares intrinsic functional architecture in humans and monkeys. Proc Natl Acad Sci USA 106:20069–20074. doi:10.1073/pnas.0905314106
McDonald CR, Crosson B, Valenstein E, Bowers D (2001) Verbal encoding deficits in a patient with a left retrosplenial lesion. Neurocase 7:407–417. doi:10.1076/neur.7.5.407.16250
Mellet E, Briscogne S, Tzourio-Mazoyer N et al (2000) Neural correlates of topographic mental exploration: the impact of route versus survey perspective learning. Neuroimage 12:588–600. doi:10.1006/nimg.2000.0648
Menon V, Uddin LQ (2010) Saliency, switching, attention and control: a network model of insula function. Brain Struct Funct 214:655–667. doi:10.1007/s00429-010-0262-0.Saliency
Milner AD, Goodale MA (2008) Two visual systems re-viewed. Neuropsychologia 46:774–785. doi:10.1016/j.neuropsychologia.2007.10.005
Poppenk J, Evensmoen HR, Moscovitch M, Nadel L (2013) Long-axis specialization of the human hippocampus. Trends Cogn Sci 17:230–240. doi:10.1016/j.tics.2013.03.005
Ridderinkhof KR (2004) The role of the medial frontal cortex in cognitive control. Science 306:443–447. doi:10.1126/science.1100301
Roth JK, Serences JT, Courtney SM (2006) Neural system for controlling the contents of object working memory in humans. Cereb Cortex 16:1595–1603. doi:10.1093/cercor/bhj096
Seghier ML (2013) The angular gyrus: multiple functions and multiple subdivisions. The Neuroscientist 19:43–61. doi:10.1177/1073858412440596
Silk TJ, Bellgrove MA, Wrafter P et al (2010) Spatial working memory and spatial attention rely on common neural processes in the intraparietal sulcus. Neuroimage 53:718–724. doi:10.1016/j.neuroimage.2010.06.068
Spiers HJ, Maguire EA (2006) Thoughts, behaviour, and brain dynamics during navigation in the real world. Neuroimage 31:1826–1840. doi:10.1016/j.neuroimage.2006.01.037
Strange BA, Dolan RJ (1999) Functional segregation within the human hippocampus. Mol Psychiatry 4:508–511
Sulpizio V, Committeri G, Lambrey S et al (2013) Selective role of lingual/parahippocampal gyrus and retrosplenial complex in spatial memory across viewpoint changes relative to the environmental reference frame. Behav Brain Res 242:62–75. doi:10.1016/j.bbr.2012.12.031
Takahashi N, Kawamura M, Shiota J et al (1997) Pure topographic disorientation due to right retrosplenial lesion. Neurology 49:464–469. doi:10.1212/WNL.49.2.464
Taube JS (1998) Head direction cells and the neurophysiological basis for a sense of direction. Prog Neurobiol 55:225–256
Valerio S, Taube JS (2012) Path integration: how the head direction signal maintains and corrects spatial orientation. Nat Neurosci 15:1445–1453. doi:10.1038/nn.3215
Vann SD, Aggleton JP, Maguire EA (2009) What does the retrosplenial cortex do? Nat Rev Neurosci 10:792–802. doi:10.1038/nrn2733
Vogt BA, Nimchinsky EA, Vogt LJ, Hof PR (1995) Human cingulate cortex: surface features, flat maps, and cytoarchitecture. J Comp Neurol 359:490–506. doi:10.1002/cne.903590310
Vogt BA, Vogt LJ, Perl DP, Hof PR (2001) Cytology of human caudomedial cingulate, retrosplenial, and caudal parahippocampal cortices. J Comp Neurol 438:353–376. doi:10.1002/cne.1320
Vogt BA, Vogt L, Laureys S (2006) Cytology and functionally correlated circuits of human posterior cingulate areas. Neuroimage 29:452–466. doi:10.1016/j.neuroimage.2005.07.048
Wagner AD, Shannon BJ, Kahn I, Buckner RL (2005) Parietal lobe contributions to episodic memory retrieval. Trends Cogn Sci 9:445–453. doi:10.1016/j.tics.2005.07.001
Wolbers T, Büchel C (2005) Dissociable retrosplenial and hippocampal contributions to successful formation of survey representations. J Neurosci 25:3333–3340. doi:10.1523/JNEUROSCI.4705-04.2005
Woollett K, Maguire EA (2009) Navigational expertise may compromise anterograde associative memory. Neuropsychologia 47:1088–1095. doi:10.1016/j.neuropsychologia.2008.12.036
Xu Y, Chun MM (2006) Dissociable neural mechanisms supporting visual short-term memory for objects. Nature 440:91–95. doi:10.1038/nature04262
Zhang S, Li C-SR (2012) Functional connectivity mapping of the human precuneus by resting state fMRI. Neuroimage 59:3548–3562. doi:10.1016/j.neuroimage.2011.11.023
Acknowledgments
This study was supported by the Natural Sciences and Engineering Research Council of Canada with a PGS-D to FB and a Discovery Grant to GI, the Killam Trusts with a Izaak Walton Killam Pre-Doctoral Scholarship to FB, and, in part, performed under a contract with Canada and the Canadian Institute for Military and Veteran Health Research.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Rights and permissions
About this article
Cite this article
Burles, F., Slone, E. & Iaria, G. Dorso-medial and ventro-lateral functional specialization of the human retrosplenial complex in spatial updating and orienting. Brain Struct Funct 222, 1481–1493 (2017). https://doi.org/10.1007/s00429-016-1288-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00429-016-1288-8