Top

Published in:

01-04-2018 | Original Article

Dual roles of the hippocampus and intraparietal sulcus in network integration and segregation support scene recognition

Authors: Xin Hao, Xu Wang, Yiying Song, Xiangzhen Kong, Jia Liu

Published in: Brain Structure and Function | Issue 3/2018

Abstract

Effectively recognizing surroundings is a critical ability in human navigation. Previous neuroimaging studies have depicted distributed brain regions underpinning spatial navigation, but little is known about how these regions are formed into the navigation network (NN) supporting scene recognition. In this study, we addressed this issue by using a voxel-based global functional connectivity method to characterize the integration (i.e., within-network connectivity, WNC) of the NN and its segregation (i.e., between-network connectivity, BNC) from non-NN networks. We found that the majority of the voxels in the NN showed a stronger WNC than BNC, indicating the encapsulation of the NN. Importantly, individuals with stronger WNC and weaker BNC in the left hippocampus (Hipp) and intraparietal sulcus (IPS) performed better in scene recognition, suggesting that the left Hipp and IPS were involved in scene recognition by both integrating regions in the NN and separating the NN from non-NN networks. Further analyses showed that the integration of these two regions in the NN serves different functions, that is, while the WNC of the left Hipp was only related to scene recognition, the WNC of the left IPS was also related to the general executive control function of attention. In short, our study demonstrated the dual roles of the Hipp and IPS in integration and segregation of the NN to support scene recognition, suggesting that scene recognition involves not only regions specialized in spatial navigation, but also those with general functions.

Available only for authorised users

Allen EA, Damaraju E, Plis SM, Erhardt EB, Eichele T, Calhoun VD (2014) Tracking whole-brain connectivity dynamics in the resting state. Cereb Cortex 24(3):663–676CrossRefPubMed

Aly M, Ranganath C, Yonelinas AP (2013) Detecting changes in scenes: the hippocampus is critical for strength-based perception. Neuron 78(6):1127–1137CrossRefPubMedPubMedCentral

Baldassano C, Beck DM, Fei-Fei L (2013) Differential connectivity within the parahippocampal place area. Neuroimage 75:228–237CrossRefPubMedPubMedCentral

Baldassano C, Esteva A, Fei-Fei L, Beck DM (2016) Two distinct scene-processing networks connecting vision and memory. eNeuro 3(5):e0178-16CrossRef

Bar M, Aminoff E (2003) Cortical analysis of visual context. Neuron 38(2):347–358CrossRefPubMed

Bird CM, Vargha-Khadem F, Burgess N (2008) Impaired memory for scenes but not faces in developmental hippocampal amnesia: a case study. Neuropsychologia 46(4):1050–1059CrossRefPubMed

Biswal BB, Mennes M, Zuo X-N, Gohel S, Kelly C, Smith SM, Beckmann CF, Adelstein JS, Buckner RL, Colcombe S (2010) Toward discovery science of human brain function. Proc Natl Acad Sci USA 107(10):4734–4739CrossRefPubMedPubMedCentral

Boccia M, Sulpizio V, Nemmi F, Guariglia C, Galati G (2017) Direct and indirect parieto-medial temporal pathways for spatial navigation in humans: evidence from resting-state functional connectivity. Brain Struct Funct 222(4):1945–1957CrossRefPubMed

Brown TI, Carr VA, LaRocque KF, Favila SE, Gordon AM, Bowles B, Bailenson JN, Wagner AD (2016) Prospective representation of navigational goals in the human hippocampus. Science 352(6291):1323–1326CrossRefPubMed

Cole MW, Yarkoni T, Repovš G, Anticevic A, Braver TS (2012) Global connectivity of prefrontal cortex predicts cognitive control and intelligence. J Neurosci 32(26):8988–8999CrossRefPubMedPubMedCentral

Dilks DD, Julian JB, Paunov AM, Kanwisher N (2013) The occipital place area is causally and selectively involved in scene perception. J Neurosci 33(4):1331–1336CrossRefPubMedPubMedCentral

Doeller CF, King JA, Burgess N (2008) Parallel striatal and hippocampal systems for landmarks and boundaries in spatial memory. Proc Natl Acad Sci USA 105(15):5915–5920CrossRefPubMedPubMedCentral

Dosenbach NU, Nardos B, Cohen AL, Fair DA, Power JD, Church JA, Nelson SM, Wig GS, Vogel AC, Lessov-Schlaggar CN (2010) Prediction of individual brain maturity using fMRI. Science 329(5997):1358–1361CrossRefPubMedPubMedCentral

Durston S, Davidson M, Thomas K, Worden M, Tottenham N, Martinez A, Watts R, Ulug A, Casey B (2003) Parametric manipulation of conflict and response competition using rapid mixed-trial event-related fMRI. Neuroimage 20(4):2135–2141CrossRefPubMed

Eickhoff SB, Stephan KE, Mohlberg H, Grefkes C, Fink GR, Amunts K, Zilles K (2005) A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data. Neuroimage 25(4):1325–1335CrossRefPubMed

Epstein R, Kanwisher N (1998) A cortical representation of the local visual environment. Nature 392(6676):598–601CrossRefPubMed

Epstein RA, Vass LK (2014) Neural systems for landmark-based wayfinding in humans. Phil Trans R Soc B 369(1635):20120533CrossRefPubMedPubMedCentral

Eriksen BA, Eriksen CW (1974) Effects of noise letters upon the identification of a target letter in a nonsearch task. Percept Psychophys 16(1):143–149CrossRef

Fair DA, Cohen AL, Power JD, Dosenbach NU, Church JA, Miezin FM, Schlaggar BL, Petersen SE (2009) Functional brain networks develop from a “local to distributed” organization. PLoS Comput Biol 5(5):e1000381CrossRefPubMedPubMedCentral

Fox MD, Snyder AZ, Vincent JL, Corbetta M, Van Essen DC, Raichle ME (2005) The human brain is intrinsically organized into dynamic, anticorrelated functional networks. Proc Natl Acad Sci USA 102(27):9673–9678CrossRefPubMedPubMedCentral

Gotts SJ, Jo HJ, Wallace GL, Saad ZS, Cox RW, Martin A (2013) Two distinct forms of functional lateralization in the human brain. Proc Natl Acad Sci USA 110(36):E3435–E3444CrossRefPubMedPubMedCentral

Grill-Spector K (2003) The neural basis of object perception. Curr Opin Neurobiol 13(2):159–166CrossRefPubMed

Hao X, Huang Y, Li X, Song Y, Kong X, Wang X, Yang Z, Zhen Z, Liu J (2016) Structural and functional neural correlates of spatial navigation: a combined voxel-based morphometry and functional connectivity study. Brain Behav 6(12):e00572CrossRefPubMedPubMedCentral

Hartley T, Maguire EA, Spiers HJ, Burgess N (2003) The well-worn route and the path less traveled: distinct neural bases of route following and wayfinding in humans. Neuron 37(5):877–888CrossRefPubMed

Hartley T, Bird CM, Chan D, Cipolotti L, Husain M, Vargha-Khadem F, Burgess N (2007) The hippocampus is required for short-term topographical memory in humans. Hippocampus 17(1):34–48CrossRefPubMedPubMedCentral

Helfinstein SM, Schonberg T, Congdon E, Karlsgodt KH, Mumford JA, Sabb FW, Cannon TD, London ED, Bilder RM, Poldrack RA (2014) Predicting risky choices from brain activity patterns. Proc Natl Acad Sci USA 111(7):2470–2475CrossRefPubMedPubMedCentral

Hodgetts C, Shine J, Lawrence A, Downing P, Graham K (2016) Evidencing a place for the hippocampus within the core scene processing network. Hum Brain Mapp 37:3779–3794CrossRefPubMedPubMedCentral

Holmes AJ, Lee PH, Hollinshead MO, Bakst L, Roffman JL, Smoller JW, Buckner RL (2012) Individual differences in amygdala-medial prefrontal anatomy link negative affect, impaired social functioning, and polygenic depression risk. J Neurosci 32(50):18087–18100CrossRefPubMedPubMedCentral

Huang L, Song Y, Li J, Zhen Z, Yang Z, Liu J (2014) Individual differences in cortical face selectivity predict behavioral performance in face recognition. Front Hum Neurosci 8:483CrossRefPubMedPubMedCentral

Jenkinson M, Smith S (2001) A global optimisation method for robust affine registration of brain images. Med Image Anal 5(2):143–156CrossRefPubMed

Jenkinson M, Bannister P, Brady M, Smith S (2002) Improved optimization for the robust and accurate linear registration and motion correction of brain images. Neuroimage 17(2):825–841CrossRefPubMed

Kong F, Chen Z, Xue S, Wang X, Liu J (2015) Mother’s but not father’s education predicts general fluid intelligence in emerging adulthood: behavioral and neuroanatomical evidence. Hum Brain Mapp 36(11):4582–4591CrossRefPubMed

Kong X-Z, Wang X, Pu Y, Huang L, Hao X, Zhen Z, Liu J (2017a) Human navigation network: the intrinsic functional organization and behavioral relevance. Brain Struct Funct 222(2):749–764CrossRefPubMed

Kong X, Song Y, Zhen Z, Liu J (2017b) Genetic variation in S100B modulates neural processing of visual scenes in Han Chinese. Cereb Cortex 27(2):1326–1336PubMed

Lauritzen T, D’Esposito M Functional networks underlying top-down visual spatial attention in the human brain. In: Soc. Neurosci. Abstr, 2007

Lebedev AV, Westman E, Simmons A, Lebedeva A, Siepel FJ, Pereira JB, Aarsland D (2014) Large-scale resting state network correlates of cognitive impairment in Parkinson’s disease and related dopaminergic deficits. Front Syst Neurosci 8:45PubMedPubMedCentral

Lever C, Wills T, Cacucci F, Burgess N, O’Keefe J (2002) Long-term plasticity in hippocampal place-cell representation of environmental geometry. Nature 416(6876):90–94CrossRefPubMed

Lew AR (2011) Looking beyond the boundaries: time to put landmarks back on the cognitive map? Psychol Bull 137(3):484CrossRefPubMed

Liang JC, Wagner AD, Preston AR (2012) Content representation in the human medial temporal lobe. Cereb Cortex 23(1):80–96CrossRefPubMedPubMedCentral

Luks TL, Simpson GV, Dale CL, Hough MG (2007) Preparatory allocation of attention and adjustments in conflict processing. Neuroimage 35(2):949–958CrossRefPubMedPubMedCentral

Maguire E (2001) The retrosplenial contribution to human navigation: a review of lesion and neuroimaging findings. Scand J Psychol 42(3):225–238CrossRefPubMed

Maguire EA, Burgess N, Donnett JG, Frackowiak RS, Frith CD, O’Keefe J (1998) Knowing where and getting there: a human navigation network. Science 280(5365):921–924CrossRefPubMed

Maguire EA, Gadian DG, Johnsrude IS, Good CD, Ashburner J, Frackowiak RS, Frith CD (2000) Navigation-related structural change in the hippocampi of taxi drivers. Proc Natl Acad Sci USA 97(8):4398–4403CrossRefPubMedPubMedCentral

Marchette SA, Vass LK, Ryan J, Epstein RA (2014) Anchoring the neural compass: coding of local spatial reference frames in human medial parietal lobe. Nature Neurosci 17(11):1598–1606CrossRefPubMedPubMedCentral

Marchette SA, Vass LK, Ryan J, Epstein RA (2015) Outside looking in: landmark generalization in the human navigational system. J Neurosci 35(44):14896–14908CrossRefPubMedPubMedCentral

Morgan LK, MacEvoy SP, Aguirre GK, Epstein RA (2011) Distances between real-world locations are represented in the human hippocampus. J Neurosci 31(4):1238–1245CrossRefPubMedPubMedCentral

Ohnishi T, Matsuda H, Hirakata M, Ugawa Y (2006) Navigation ability dependent neural activation in the human brain: an fMRI study. Neurosci Res 55(4):361–369CrossRefPubMed

O’Keefe J, Dostrovsky J (1971) The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. Brain Res 34(1):171–175CrossRefPubMed

Peschke C, Köster R, Korsch M, Frühholz S, Thiel CM, Herrmann M, Hilgetag CC (2016) Selective perturbation of cognitive conflict in the human brain—a combined fMRI and rTMS study. Sci Rep 6:38700CrossRefPubMedPubMedCentral

Poppenk J, Evensmoen HR, Moscovitch M, Nadel L (2013) Long-axis specialization of the human hippocampus. Trends Cogn Sci 17(5):230–240CrossRefPubMed

Posner MI, Petersen SE (1990) The attention system of the human brain. Annu Rev Neurosci 13(1):25–42CrossRefPubMed

Power JD, Barnes KA, Snyder AZ, Schlaggar BL, Petersen SE (2012) Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion. Neuroimage 59(3):2142–2154CrossRefPubMed

Raven JC, Court JH (1998) Raven’s progressive matrices and vocabulary scales. Oxford Psychologists Press, Oxford

Rubinov M, Sporns O (2010) Complex network measures of brain connectivity: uses and interpretations. Neuroimage 52(3):1059–1069CrossRefPubMed

Ryals AJ, Wang JX, Polnaszek KL, Voss JL (2015) Hippocampal contribution to implicit configuration memory expressed via eye movements during scene exploration. Hippocampus 25(9):1028–1041CrossRefPubMedPubMedCentral

Schindler A, Bartels A (2013) Parietal cortex codes for egocentric space beyond the field of view. Curr Biol 23(2):177–182CrossRefPubMed

Silson EH, Steel AD, Baker CI (2016) Scene-selectivity and retinotopy in medial parietal cortex. Front Hum Neurosci 10:1–17CrossRef

Silver MA, Ress D, Heeger DJ (2005) Topographic maps of visual spatial attention in human parietal cortex. J Neurophysiol 94(2):1358–1371CrossRefPubMedPubMedCentral

Soutschek A, Taylor PC, Müller HJ, Schubert T (2013) Dissociable networks control conflict during perception and response selection: a transcranial magnetic stimulation Study. J Neurosci 33(13):5647–5654CrossRefPubMed

Spelke ES, Lee SA (2012) Core systems of geometry in animal minds. Philos Trans R Soc B 367(1603):2784–2793CrossRef

Spiers HJ, Maguire EA (2006) Thoughts, behaviour, and brain dynamics during navigation in the real world. Neuroimage 31(4):1826–1840CrossRefPubMed

Sporns O (2013) Network attributes for segregation and integration in the human brain. Curr Opin Neurobiol 23(2):162–171CrossRefPubMed

Sulpizio V, Boccia M, Guariglia C, Galati G (2016) Functional connectivity between posterior hippocampus and retrosplenial complex predicts individual differences in navigational ability. Hippocampus 26(7):841–847CrossRefPubMed

Summerfield JJ, Hassabis D, Maguire EA (2010) Differential engagement of brain regions within a ‘core’network during scene construction. Neuropsychologia 48(5):1501–1509CrossRefPubMedPubMedCentral

Supekar K, Musen M, Menon V (2009) Development of large-scale functional brain networks in children. PLoS Biol 7(7):e1000157CrossRefPubMedPubMedCentral

Taylor KJ, Henson RN, Graham KS (2007) Recognition memory for faces and scenes in amnesia: dissociable roles of medial temporal lobe structures. Neuropsychologia 45(11):2428–2438CrossRefPubMed

Uttal DH, Sandstrom LB, Newcombe NS (2006) One hidden object, two spatial codes: young children’s use of relational and vector coding. J Cogn Dev 7(4):503–525CrossRef

Vass LK, Epstein RA (2013) Abstract representations of location and facing direction in the human brain. J Neurosci 33(14):6133–6142CrossRefPubMedPubMedCentral

Wang L, Mruczek RE, Arcaro MJ, Kastner S (2014) Probabilistic maps of visual topography in human cortex. Cereb Cortex 25(10):3911–3931CrossRefPubMedPubMedCentral

Wang X, Song Y, Zhen Z, Liu J (2016a) Functional integration of the posterior superior temporal sulcus correlates with facial expression recognition. Hum Brain Mapp 37:1930–1940CrossRefPubMed

Wang X, Zhen Z, Song Y, Huang L, Kong X, Liu J (2016b) The hierarchical structure of the face network revealed by its functional connectivity pattern. J Neurosci 36(3):890–900CrossRefPubMed

Wegman J, Tyborowska A, Janzen G (2014) Encoding and retrieval of landmark-related spatial cues during navigation: an fMRI study. Hippocampus 24(7):853–868CrossRefPubMed

Weiner KS, Barnett M, Witthoft N, Golarai G, Stigliani A, Kay KN, Gomez J, Natu VS, Amunts K, Zilles K (2017) Defining the most probable location of the parahippocampal place area using cortex-based alignment and cross-validation. Neuroimage. https://doi.org/10.1016/j.neuroimage.2017.04.040

Whitlock JR, Sutherland RJ, Witter MP, Moser M-B, Moser EI (2008) Navigating from hippocampus to parietal cortex. Proc Natl Acad Sci USA 105(39):14755–14762CrossRefPubMedPubMedCentral

Wolbers T, Hegarty M (2010) What determines our navigational abilities? Trends Cogn Sci 14(3):138–146CrossRefPubMed

Woollett K, Maguire EA (2011) Acquiring “the knowledge” of London’s layout drives structural brain changes. Curr Biol 21(24):2109–2114CrossRefPubMedPubMedCentral

Woolley DG, Mantini D, Coxon JP, D’Hooge R, Swinnen SP, Wenderoth N (2015) Virtual water maze learning in human increases functional connectivity between posterior hippocampus and dorsal caudate. Hum Brain Mapp 36(4):1265–1277CrossRefPubMed

Yarkoni T, Poldrack RA, Nichols TE, Van Essen DC, Wager TD (2011) Large-scale automated synthesis of human functional neuroimaging data. Nat Methods 8(8):665–670CrossRefPubMedPubMedCentral

Zeidman P, Mullally SL, Maguire EA (2015) Constructing, perceiving, and maintaining scenes: hippocampal activity and connectivity. Cereb Cortex 25(10):3836–3855CrossRefPubMed

Zhen Z, Yang Z, Huang L, Kong X, Wang X, Dang X, Huang Y, Song Y, Liu J (2015) Quantifying interindividual variability and asymmetry of face-selective regions: a probabilistic functional atlas. Neuroimage 113:13–25CrossRefPubMed

Zhen Z, Kong XZ, Huang L, Yang Z, Wang X, Hao X, Huang T, Song Y, Liu J (2017) Quantifying the variability of scene-selective regions: interindividual, interhemispheric, and sex differences. Hum Brain Mapp 38(4):2260–2275CrossRefPubMed

Title: Dual roles of the hippocampus and intraparietal sulcus in network integration and segregation support scene recognition
Authors: Xin Hao
Xu Wang
Yiying Song
Xiangzhen Kong
Jia Liu
Publication date: 01-04-2018
Publisher: Springer Berlin Heidelberg
Published in: Brain Structure and Function / Issue 3/2018
Print ISSN: 1863-2653
Electronic ISSN: 1863-2661
DOI: https://doi.org/10.1007/s00429-017-1564-2

Keynote webinar | Spotlight on sleep in brain health

Springer Medicine

Dual roles of the hippocampus and intraparietal sulcus in network integration and segregation support scene recognition

Abstract

Keynote webinar | Spotlight on sleep in brain health

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 3/2018

The effect of inhibition on stimulus-specific adaptation in the inferior colliculus

Oligomer-prone E57K-mutant alpha-synuclein exacerbates integration deficit of adult hippocampal newborn neurons in transgenic mice

Perineuronal nets labeled by monoclonal antibody VC1.1 ensheath interneurons expressing parvalbumin and calbindin in the rat amygdala

High-resolution language mapping of Broca’s region with transcranial magnetic stimulation

Functional rostro-caudal gradient in the human posterior lateral frontal cortex

Multi-scale account of the network structure of macaque visual cortex