Abstract
Anatomical and functional findings in primates suggest the existence of a dedicated parieto-medial temporal pathway for spatial navigation, consisting of both direct and indirect projections from the caudal inferior parietal lobe (cIPL) to the hippocampus and the parahippocampal cortex, with indirect projections relaying through the posterior cingulate and retrosplenial cortex. This neural network is largely unexplored in humans. This study aimed at testing the existence of a parieto-medial temporal pathway for spatial navigation in humans. We explored the cortical connectivity patterns of the parahippocampal place area (PPA), the retrosplenial cortex (RSC), and the hippocampus (HC) using resting-state functional connectivity MRI. Our results demonstrate the existence of connections between the medial temporal lobe structures, i.e., PPA and HC, and the angular gyrus (AG), the human homologue of cIPL, as well as between RSC and AG. These connectivity patterns seem to reflect the direct and the indirect projections found in primates from cIPL to the medial temporal lobe. Such a result deserves feasible considerations to better understand the brain networks underpinning human spatial navigation.
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References
Aguirre GK, Esposito MD (1999) Topographical disorientation: a synthesis and taxonomy. Brain 122:1613–1628
Boccia M, Nemmi F, Guariglia C (2014) Neuropsychology of environmental navigation in humans: review and meta-analysis of FMRI studies in healthy participants. Neuropsychol Rev 24(2):236–251. doi:10.1007/s11065-014-9247-8
Boccia M, Guariglia C, Sabatini U, Nemmi F (2015a) Navigating toward a novel environment from a route or survey perspective: neural correlates and context-dependent connectivity. Brain Struct Funct. doi:10.1007/s00429-015-1021-z
Boccia M, Piccardi L, Palermo L, Nemmi F, Sulpizio V, Galati G, Guariglia C (2015b) A penny for your thoughts! patterns of fMRI activity reveal the content and the spatial topography of visual mental images. Hum Brain Mapp 36(3):945–958. doi:10.1002/hbm.22678
Buckner RL, Krienen FM, Yeo BTT (2013) Opportunities and limitations of intrinsic functional connectivity MRI. Nat Neurosci 16:832–837. doi:10.1038/nn.3423
Byrne P, Becker S, Burgess N (2007) Remembering the past and imagining the future: a neural model of spatial memory and imagery. Psychol Rev 114:340–375. doi:10.1037/0033-295X.114.2.340
Cavada C, Goldman-Rakic PS (1989) Posterior parietal cortex in rhesus monkey: I. Parcellation of areas based on distinctive limbic and sensory corticocortical connections. J Comp Neurol 287:393–421
Cherney ID, Brabec CM, Runco DV (2008) Mapping out spatial ability: sex differences in way-finding navigation. Percept Mot Skills 107:747–760
Clark BJ, Bassett JP, Wang SS, Taube JS (2010) Impaired head direction cell representation in the anterodorsal thalamus after lesions of the retrosplenial cortex. J Neurosci 30(15):5289–5302. doi:10.1523/JNEUROSCI.3380-09.2010
Committeri G, Piccardi L, Galati G, Guariglia C (2015) Where did you “left” Piazza del Popolo? At your “right” temporo-parietal junction. Cortex 73:106–111
Ding SL, Van Hoesen G, Rockland KS (2000) Inferior parietal lobule projections to the presubiculum and neighboring ventromedial temporal cortical areas. J Comp Neurol 425:510–530
Eichenbaum H, Cohen NJ (2001) From conditioning to conscious recollection: memory systems of the brain. Oxford University, Upper Saddle River
Eichenbaum H, Sauvage M, Fortin N, Komorowski R, Lipton P (2012) Towards a functional organization of episodic memory in the medial temporal lobe. Neurosci Biobehav Rev 36(7):1597–1608
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
Epstein R, Harris A, Stanley D, Kanwisher N (1999) The parahippocampal place area: recognition, navigation, or encoding? Neuron 23:115–125. doi:10.1016/S0896-6273(00)80758-8
Fox MD, Raichle ME (2007) Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging. Nat Rev Neurosci 8:700–711. doi:10.1038/nrn2201
Friston KJ, Holmes A, Poline JB, Price CJ, Frith CD (1996) Detecting activations in PET and fMRI: levels of inference and power. Neuroimage 4:223–235. doi:10.1006/nimg.1996.0074
Ganesh S, van Schie HT, Cross ES, de Lange FP, Wigboldus DH (2015) Disentangling neural processes of egocentric and allocentric mental spatial transformations using whole-body photos of self and other. Neuroimage 116:30–39. doi:10.1016/j.neuroimage.2015.05.003 (Epub 2015 May 12)
Genovesio A, Ferraina S (2004) Integration of retinal disparity and fixation-distance related signals toward an egocentric coding of distance in the posterior parietal cortex of primates. J Neurophysiol 91:2670–2684. doi:10.1152/jn.00712.2003
Georgieva S, Peeters R, Kolster H, Todd JT, Orban GA (2009) The processing of three-dimensional shape from disparity in the human brain. J Neurosci 29:727–742. doi:10.1523/JNEUROSCI.4753-08.2009
Ghaem O, Mellet E, Crivello F, Tzourio N, Mazoyer B, Berthoz A, Denis M (1997) Mental navigation along memorized routes activates the hippocampus, precuneus, and insula. Neuroreport 8:739–744. doi:10.1097/00001756-199702100-00032
Grön G, Wunderlich AP, Spitzer M, Tomczak R, Riepe MW (2000) Brain activation during human navigation: gender-different neural networks as substrate of performance. Nat Neurosci 3(4):404–408
Guariglia C, Piccardi L (2010) Environmental orientation and navigation in different types of unilateral neglect. Exp Brain Res 206(2):163–169
Guariglia C, Piccardi L, Iaria G, Nico D, Pizzamiglio L (2005) Representational neglect and navigation in real space. Neuropsychologia 43(8):1138–1143
Habib M, Sirigu A (1987) Pure topographical disorientation: a definition and anatomical basis. Cortex 23:73–85
Hafting T, Fyhn M, Molden S, Moser M-B, Moser EI (2005) Microstructure of a spatial map in the entorhinal cortex. Nature 436 (7052):801–806. doi:http://www.nature.com/nature/journal/v436/n7052/suppinfo/nature03721_S1.html
Iaria G, Chen JK, Guariglia C, Ptito A, Petrides M (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, Hirose S, Kimura T, Fukuyama H (2002) Mental navigation in humans is processed in the anterior bank of the parieto-occipital sulcus. Neurosci Lett. doi:10.1016/S0304-3940(02)00019-8
Kaski D, Quadir S, Nigmatullina Y, Malhotra PA, Bronstein AM, Seemungal BM (2016) Temporoparietal encoding of space and time during vestibular-guided orientation. Brain. doi:10.1093/brain/awv370
Kim S, Sapiurka M, Clark RE, Squire LR (2013) Contrasting effects on path integration after hippocampal damage in humans and rats. PNAS 110(12):4732–4737. doi:10.1073/pnas.1300869110 (Epub 2013 Feb 12)
Kim S, Dede AJ, Hopkins RO, Squire LR (2015) Memory, scene construction, and the human hippocampus. PNAS 112(15):4767–4772. doi:10.1073/pnas.1503863112 (Epub 2015 Mar 30)
Kobayashi Y, Amaral DG (2003) Macaque monkey retrosplenial cortex: II. Cortical afferents. J Comp Neurol 466:48–79
Kobayashi Y, Amaral DG (2007) Macaque monkey retrosplenial cortex: III. Cortical efferents. J Comp Neurol 502:810–833
Kravitz DJ, Saleem KS, Baker CI, Mishkin M (2011) A new neural framework for visuospatial processing. Nat Rev Neurosci 12:217–230. doi:10.1167/11.11.923
Lambrey S, Doeller C, Berthoz A, Burgess N (2012) Imagining being somewhere else: neural basis of changing perspective in space. Cereb Cortex 22:166–174. doi:10.1093/cercor/bhr101
Lipton PA, Eichenbaum (2008) Complementary roles of hippocampus and medial entorhinal cortex in episodic memory. Neural Plasticity. doi:10.1155/2008/258467
Macko KA, Jarvis CD, Kennedy C, Miyaoka M, Shinohara M, Sololoff L, Mishkin M (1982) Mapping the primate visual system with [2-14C]deoxyglucose. Science (New York, NY) 218:394–397. doi:10.1126/science.7123241
Maguire EA (1998) Knowing where and getting there: a human navigation network. Science 280:921–924. doi:10.1126/science.280.5365.921
Maguire EA, Intraub H, Mullally SL (2015) Scenes, spaces, and memory traces: what does the hippocampus do? Neuroscientist. doi:10.1177/1073858415600389
Margulies DS, Vincent JL, Kelly C, Lohmann G, Uddin LQ, Biswal BB (2009) Precuneus shares intrinsic functional architecture in humans and monkeys:106
Mazziotta JC, Toga AW, Evans A, Fox P, Lancaster J (1995) A probabilistic atlas of the human brain: theory and rationale for its development. The International Consortium for Brain Mapping (ICBM). Neuroimage 2:89–101. doi:10.1006/nimg.1995.1012
Milner B (2005) The medial temporal-lobe amnesic syndrome. Psychiatr Clin N Am 28(3):599–611. doi:10.1016/j.psc.2005.06.002.609
Milner AD, Goodale MA (1995) The visual brain in action. Oxford University Press, Oxford
Mishkin M, Ungerleider LG, Macko KA (1983) Object vision and spatial vision: two cortical pathways. Trends Neurosci. doi:10.1016/0166-2236(83)90190-X
Morgan LK, Macevoy SP, Aguirre GK, Epstein RA (2011) Distances between real-world locations are represented in the human hippocampus. J Neurosci 31:1238–1245. doi:10.1523/JNEUROSCI.4667-10.2011
Morris R, Pandya DN, Petrides M (1999) Fiber systemlinking the mid-dorsolateral frontal cortex with the retrosplenial/presubicular region in the rhesus monkey. J Comp Neurol 407:183–192
Nemmi F, Boccia M, Piccardi L, Galati G, Guariglia C (2013) Segregation of neural circuits involved in spatial learning in reaching and navigational space. Neuropsychologia 51(8):1561–1570. doi:10.1016/j.neuropsychologia.2013.03.031
Nico D, Piccardi L, Iaria G, Bianchini F, Zompanti L, Guariglia C (2008) Landmark based navigation in brain-damaged patients with neglect. Neuropsychologia 46(7):1898–1907
O’Keefe J, Nadel L (1979) Précis of O’Keefe and Nadel’s The hippocampus as a cognitive map. Behav Brain Sci. doi:10.1017/S0140525X00063949
Persson J, Herlitz A, Engman J, Morell A, Sjölie D, Wikström J, Söderlund H (2013) Remembering our origin: gender differences in spatial memory are reflected in gender differences in hippocampal lateralization. Behav Brain Res 256:219–228
Philbeck JW, Behrmann M, Loomis JM (2001) Updating of locations during whole-body rotations in patients with hemispatial neglect. Cogn Affect Behav Neurosci 1:330–343
Piccardi L, Bianchini F, Iasevoli L, Giannone G, Guariglia C (2011) Sex differences in a landmark environmental re-orientation task only during the learning phase. Neurosci Lett 503(3):181–185
Pitzalis S, Galletti C, Huang RS, Patria F, Committeri G, Galati G, Fattori P, Sereno MI (2006) Wide-field retinotopy defines human cortical visual area v6. J Neurosci 26(30):7962–7973
Pitzalis S, Sereno MI, Committeri G, Fattori P, Galati G, Tosoni A, Galletti C (2013) The human homologue of macaque area V6A. Neuroimage 82:517–530. doi:10.1016/j.neuroimage.2013.06.026
Rockland KS, Van Hoesen GW (1999) Some temporal and parietal cortical connections converge in CA1 of the primate hippocampus. Cereb Cortex 9:232–237
Schindler A, Bartels A (2013) Parietal cortex codes for egocentric space beyond the field of view. Curr Biol 23:177–182. doi:10.1016/j.cub.2012.11.060
Sereno MI, Huang RS (2006) A human parietal face area contains aligned head-centered visual and tactile maps. Nat Neurosci 9:1337–1343. doi:10.1038/nn1777
Squire LR (1992) Memory and the hippocampus: a synthesis from findings with rats, monkeys, and humans. Psychol Rev 99(2):195–231
Squire LR, Wixted JT (2011) The cognitive neuroscience of human memory since H.M. Annu Rev Neurosci 34:259–288
Stark M, Coslett HB, Saffran EM (1996) Impairment of an egocentric map of locations: implications for perception and action. Cogn Neuropsychol 13:481–523
Sulpizio V, Committeri G, Lambrey S, Berthoz A, Galati G (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
Sulpizio V, Committeri G, Galati G (2014) Distributed cognitive maps reflecting real distances between places and views in the human brain. Front Hum Neurosci 8:716. doi:10.3389/fnhum.2014.00716
Sulpizio V, Boccia M, Guariglia C, Galati G (2016a) Functional connectivity between posterior hippocampus and retrosplenial complex predicts individual differences in navigational ability. Hippocampus 26(7):841–847. doi:10.1002/hipo.22592
Sulpizio V, Committeri G, Lambrey S, Berthoz A, Galati G (2016b) Role of the human retrosplenial cortex/parieto-occipital sulcus in perspective priming. Neuroimage 125:108–119. doi:10.1016/j.neuroimage.2015.10.040
Takahashi N, Kawamura M, Shiota J, Kasahata N, Hirayama K (1997) Pure topographic disorientation due to right retrosplenial lesion. Neurology 49:464–469
Tosoni A, Corbetta M, Calluso C, Committeri G, Pezzulo G, Romani GL, Galati G (2014) Decision and action planning signals in human posterior parietal cortex during delayed perceptual choices. Eur J Neurosci 39(8):1370–1383. doi:10.1111/ejn.12511
Tosoni A, Pitzalis S, Committeri G, Fattori P, Galletti C, Galati G (2015) Resting-state connectivity and functional specialization in human medial parieto-occipital cortex. Brain Struct Funct 220:3307–3321. doi:10.1007/s00429-014-0858-x
Ungerleider LG, Mishkin M (1982) Analysis of visual behavior. Technology. doi:10.1038/nrmicro1558
Vass LK, Epstein Ra (2013) Abstract representations of location and facing direction in the human brain. J Neurosci 33:6133–6142. doi:10.1523/JNEUROSCI.3873-12.2013
Verde P, Piccardi L, Bianchini F, Guariglia C, Carrozzo P, Morgagni F, Boccia M, Di Fiore G, Tomao E (2015) Gender differences in navigational memory: pilots vs. non pilots. Aerosp Med Hum Perform 86(2):103–111
Wall MB, Smith AT (2008) The representation of egomotion in the human brain. Curr Biol 18(3):191–194. doi:10.1016/j.cub.2007.12.053
Wu J, Yan T, Zhang Z, Jin F, Guo Q (2012) Retinotopic mapping of the peripheral visual field to human visual cortex by functional magnetic resonance imaging. Hum Brain Mapp 33:1727–1740. doi:10.1002/hbm.21324
Yarkoni T, Poldrack RA, Nichols TE, Van Essen DC, Wager T (2011) Large-scale automated synthesis of human functional neuroimaging data. Nat Methods 8:665–670
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Boccia, M., Sulpizio, V., Nemmi, F. et al. Direct and indirect parieto-medial temporal pathways for spatial navigation in humans: evidence from resting-state functional connectivity. Brain Struct Funct 222, 1945–1957 (2017). https://doi.org/10.1007/s00429-016-1318-6
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DOI: https://doi.org/10.1007/s00429-016-1318-6