Abstract
The relationship between the local morphological features that define the entorhinal and parahippocampal cortex in the medial temporal region of the human brain and activation as measured during a navigation task with functional magnetic resonance imaging was examined individually in healthy participants. Two functional activation clusters were identified one within the caudal end of the collateral sulcus proper and the other in the parahippocampal extension of the collateral sulcus, clearly establishing the activation in the posterior parahippocampal cortex. A third activation cluster was identified where the anterior segment of the collateral sulcus proper gives way to the posterior segment, demonstrating also activation within the middle parahippocampal cortex. No activation was observed in the entorhinal cortex that lies medial to the rhinal sulcus or in the anterior part of the parahippocampal cortex along the anterior branch of the collateral sulcus proper. The activations could also be clearly differentiated from the cortex of the fusiform and lingual gyri that lie laterally and posteriorly. These findings demonstrated specific activation in the middle and posterior part of the parahippocampal cortex when information necessary for navigation was retrieved from a previously established cognitive map and demonstrate that the sulci that comprise the collateral sulcal complex represent important landmarks that can provide an accurate localization of activation foci along the parahippocampal cortex and allow identification of subdivisions involved in the processing of spatial information.
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References
Aguirre GK, D’Esposito M (1997) Environmental knowledge is subserved by separable dorsal/ventral neural areas. J Neurosci 17:2512–2518
Aguirre GK, Detre JA, Alsop DC, D’Esposito M (1996) The parahippocampus subserves topographical learning in man. Cereb Cortex 6:823–829. doi:10.1093/cercor/6.6.823
Aguirre GK, Zarahn E, D’Esposito M (1998) An area within human ventral cortex sensitive to “building” stimuli: evidence and implications. Neuron 21:373–383
Amiez C, Petrides M (2014) Neuroimaging evidence of the anatomo-functional organization of the human cingulate motor areas. Cereb Cortex 24:563–578. doi:10.1093/cercor/bhs329
Amiez C, Kostopoulos P, Champod AS, Petrides M (2006) Local morphology predicts functional organization of the dorsal premotor region in the human brain. J Neurosci 26:2724–2731. doi:10.1523/JNEUROSCI.4739-05.2006
Aminoff E, Gronau N, Bar M (2007) The parahippocampal cortex mediates spatial and nonspatial associations. Cereb Cortex 17:1493–1503. doi:10.1093/cercor/bhl078
Andrews TJ, Clarke A, Pell P, Hartley T (2010) Selectivity for low-level features of objects in the human ventral stream. NeuroImage 49:703–711. doi:10.1016/j.neuroimage.2009.08.046
Arcaro MJ, McMains SA, Singer BD, Kastner S (2009) Retinotopic organization of human ventral visual cortex. J Neurosci 29:10638–10652. doi:10.1523/JNEUROSCI.2807-09.2009
Arnold AE, Protzner AB, Bray S, Levy RM, Iaria G (2014) Neural network configuration and efficiency underlies individual differences in spatial orientation ability. J Cogn Neurosci 26:380–394. doi:10.1162/jocn_a_00491
Bachevalier J, Nemanic S (2008) Memory for spatial location and object-place associations are differently processed by the hippocampal formation, parahippocampal areas TH/TF and perirhinal cortex. Hippocampus 18:64–80. doi:10.1002/hipo.20369
Baldassano C, Beck DM, Fei-Fei L (2013) Differential connectivity within the parahippocampal place area. NeuroImage 75:228–237
Bohbot VD, Kalina M, Stepankova K, Spackova N, Petrides M, Nadel L (1998) Spatial memory deficits in patients with lesions to the right hippocampus and to the right parahippocampal cortex. Neuropsychologia 36:1217–1238
Buffalo EA, Bellgowan PS, Martin A (2006) Distinct roles for medial temporal lobe structures in memory for objects and their locations. Learn Mem 13:638–643. doi:10.1101/lm.251906
Collins DL, Neelin P, Peters TM, Evans AC (1994) Automatic 3D intersubject registration of MR volumetric data in standardized Talairach space. J Comput Assist Tomogr 18:192–205
Epstein RA (2008) Parahippocampal and retrosplenial contributions to human spatial navigation. Trends Cognit Sci 12:388–396. doi:10.1016/j.tics.2008.07.004
Epstein R, Kanwisher N (1998) A cortical representation of the local visual environment. Nature 392:598–601
Friston KJ, Fletcher P, Josephs O, Holmes A, Rugg MD, Turner R (1998) Event-related fMRI: characterizing differential responses. NeuroImage 7:30–40. doi:10.1006/nimg.1997.0306
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 436:801–806
Huntgeburth SC, Petrides M (2012) Morphological patterns of the collateral sulcus in the human brain. Eur J Neurosci 35:1295–1311. doi:10.1111/j.1460-9568.2012.08031.x
Huntgeburth SC, Petrides M (2016) Three-dimensional probability maps of the rhinal and the collateral sulci in the human brain. Brain Struct Funct. doi:10.1007/s00429-016-1189-x
Iaria G, Petrides M, Dagher A, Pike B, Bohbot VD (2003) Cognitive strategies dependent on the hippocampus and caudate nucleus in human navigation: variability and change with practice. J Neurosci 23(13):5945–5952
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
Iaria G, Fox CJ, Chen J-K, Petrides M, Barton JJS (2008) Detection of unexpected events during spatial navigation in humans: bottom-up attentional system and neural mechanisms. Eur J Neurosci 27:1017–1025. doi:10.1111/j.1460-9568.2008.06060.x
Jacobs J, Weidemann CT, Miller JF, Solway A, Burke JF, Wei X-X, Suthana N, Sperling MR, Sharan AD, Fried I, Kahana MJ (2013) Direct recordings of grid-like neuronal activity in human spatial navigation. Nat Neurosci 16:1188–1190
Köhler S, Crane J, Milner B (2002) Differential contributions of the parahippocampal place area and the anterior hippocampus to human memory for scenes. Hippocampus 12:718–723. doi:10.1002/hipo.10077
Litman L, Awipi T, Davachi L (2009) Category-specificity in the human medial temporal lobe cortex. Hippocampus 19:308–319. doi:10.1002/hipo.20515
Lovell MR, Collins MW (1998) Neuropsychological assessment of the college football player. J Head Trauma Rehabil 13:9–26
Malkova L, Mishkin M (2003) One-trial memory for object-place associations after separate lesions of hippocampus and posterior parahippocampal region in the monkey. J Neurosci 23:1956–1965
Pihlajamaki M, Tanila H, Kononen M, Hanninen T, Hamalainen A, Soininen H, Aronen HJ (2004) Visual presentation of novel objects and new spatial arrangements of objects differentially activates the medial temporal lobe subareas in humans. Eur J Neurosci 19:1939–1949. doi:10.1111/j.1460-9568.2004.03282.x
Ploner CJ, Gaymard BM, Rivaud-Pechoux S, Baulac M, Clemenceau S, Samson S, Pierrot-Deseilligny C (2000) Lesions affecting the parahippocampal cortex yield spatial memory deficits in humans. Cereb Cortex 10:1211–1216
Raichle ME, MacLeod AM, Snyder AZ, Powers WJ, Gusnard DA, Shulman GL (2001) A default mode of brain function. PNAS 98(2):676–682
Sato N, Nakamura K (2003) Visual response properties of neurons in the parahippocampal cortex of monkeys. J Neurophysiol 90:876–886. doi:10.1152/jn.01089.2002
Scoville WB, Milner B (1957) Loss of recent memory after bilateral hippocampal lesions. J Neurol Neurosurg Psychiatry 20:11–21
Segal E, Petrides M (2013) Functional activation during reading in relation to the sulci of the angular gyrus region. Eur J Neurosci 38:2793–2801. doi:10.1111/ejn.12277
Smith ML, Milner B (1981) The role of the right hippocampus in the recall of spatial location. Neuropsychologia 19:781–793
Squire LR, Zola-Morgan S (1991) The medial temporal lobe memory system. Science (New York, NY) 253:1380–1386
Staresina BP, Duncan KD, Davachi L (2011) Perirhinal and parahippocampal cortices differentially contribute to later recollection of object- and scene-related event details. J Neurosci 31:8739–8747. doi:10.1523/JNEUROSCI.4978-10.2011
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
Van Hoesen GW (1982) The parahippocampal gyrus: new observations regarding its cortical connections in the monkey. Trends Neurosci 5:345–350
Van Hoesen GW (1995) Anatomy of the medial temporal lobe. Magn Reson Imaging 13:1047–1055
Van Hoesen GW, Pandya DN, Butters N (1972) Cortical afferents to the entorhinal cortex of the Rhesus monkey. Science 175:1471–1473
Worsley KJ, Liao C, Aston J, Petre V, Duncan GH, Morales F, Evans AC (2002) A general statistical analysis for fMRI data. NeuroImage 15:1–15
Xu J, Evensmoen HR, Lehn H, Pintzka CW, Haberg AK (2010) Persistent posterior and transient anterior medial temporal lobe activity during navigation. NeuroImage 52:1654–1666. doi:10.1016/j.neuroimage.2010.05.074
Yousry TA, Schmid UD, Alkadhi H, Schmidt D, Peraud A, Buettner A, Winkler P (1997) Localization of the motor hand area to a knob on the precentral gyrus, a new landmark. Brain 120:141–157
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The authors thank Rhonda Amsel and Veronika Zlatkina for helpful discussions on the project.
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The authors declare that they have no competing financial or non-financial interests. All research was conducted in compliance with ethical standards.
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All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.
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The research was supported by the Canadian Institutes of Health Research (CIHR) grant MOP-64271 to AP and MP, and CIHR Foundation FDN-143212 grant to MP.
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Huntgeburth, S.C., Chen, JK., Ptito, A. et al. Local morphology informs location of activation during navigation within the parahippocampal region of the human brain. Brain Struct Funct 222, 1581–1596 (2017). https://doi.org/10.1007/s00429-016-1293-y
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DOI: https://doi.org/10.1007/s00429-016-1293-y