Functional topography of the human entorhinal cortex

Despite extensive research on the role of the rodent medial and lateral entorhinal cortex (MEC/LEC) in spatial navigation, memory and related disease, their human homologues remain elusive. Here, we combine high-field functional magnetic resonance imaging at 7 T with novel data-driven and model-based analyses to identify corresponding subregions in humans based on the well-known global connectivity fingerprints in rodents and sensitivity to spatial and non-spatial information. We provide evidence for a functional division primarily along the anteroposterior axis. Localising the human homologue of the rodent MEC and LEC has important implications for translating studies on the hippocampo-entorhinal memory system from rodents to humans. DOI: http://dx.doi.org/10.7554/eLife.06738.001

[1]  M. Witter,et al.  Functional organization of the extrinsic and intrinsic circuitry of the parahippocampal region , 1989, Progress in Neurobiology.

[2]  D. Ts'o,et al.  Functional organization of primate visual cortex revealed by high resolution optical imaging. , 1990, Science.

[3]  H. Braak,et al.  The human entorhinal cortex: normal morphology and lamina-specific pathology in various diseases , 1992, Neuroscience Research.

[4]  W. Suzuki,et al.  Topographic organization of the reciprocal connections between the monkey entorhinal cortex and the perirhinal and parahippocampal cortices , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[5]  R. Saunders,et al.  The entorhinal cortex: an examination of cyto- and myeloarchitectonic organization in humans. , 1997, Cerebral cortex.

[6]  Nancy Kanwisher,et al.  A cortical representation of the local visual environment , 1998, Nature.

[7]  H. Soininen,et al.  MR volumetric analysis of the human entorhinal, perirhinal, and temporopolar cortices. , 1998, AJNR. American journal of neuroradiology.

[8]  Mikhail Belkin,et al.  Laplacian Eigenmaps for Dimensionality Reduction and Data Representation , 2003, Neural Computation.

[9]  Jason P. Mitchell,et al.  Multiple routes to memory: Distinct medial temporal lobe processes build item and source memories , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[10]  Timothy Edward John Behrens,et al.  Changes in connectivity profiles define functionally distinct regions in human medial frontal cortex. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[11]  T. Hafting,et al.  Microstructure of a spatial map in the entorhinal cortex , 2005, Nature.

[12]  R. Insausti,et al.  Cortical efferents of the entorhinal cortex and the adjacent parahippocampal region in the monkey (Macaca fascicularis) , 2005, The European journal of neuroscience.

[13]  Guido Gerig,et al.  User-guided 3D active contour segmentation of anatomical structures: Significantly improved efficiency and reliability , 2006, NeuroImage.

[14]  Torkel Hafting,et al.  Conjunctive Representation of Position, Direction, and Velocity in Entorhinal Cortex , 2006, Science.

[15]  Arne D. Ekstrom,et al.  Spatial and temporal episodic memory retrieval recruit dissociable functional networks in the human brain. , 2007, Learning & memory.

[16]  Kara L. Agster,et al.  Functional neuroanatomy of the parahippocampal region in the rat: The perirhinal and postrhinal cortices , 2007, Hippocampus.

[17]  D. Amaral,et al.  Entorhinal cortex of the monkey: VII. Intrinsic connections , 2007, The Journal of comparative neurology.

[18]  Kara L. Agster,et al.  Functional neuroanatomy of the parahippocampal region: The lateral and medial entorhinal areas , 2007, Hippocampus.

[19]  H. Eichenbaum,et al.  The medial temporal lobe and recognition memory. , 2007, Annual review of neuroscience.

[20]  Damien A. Fair,et al.  Defining functional areas in individual human brains using resting functional connectivity MRI , 2008, NeuroImage.

[21]  M. Witter,et al.  What Does the Anatomical Organization of the Entorhinal Cortex Tell Us? , 2008, Neural plasticity.

[22]  H. Eichenbaum,et al.  Towards a functional organization of the medial temporal lobe memory system: Role of the parahippocampal and medial entorhinal cortical areas , 2008, Hippocampus.

[23]  D. Amaral,et al.  Entorhinal cortex of the monkey: IV. Topographical and laminar organization of cortical afferents , 2008, The Journal of comparative neurology.

[24]  Christian F. Doeller,et al.  Parallel striatal and hippocampal systems for landmarks and boundaries in spatial memory , 2008, Proceedings of the National Academy of Sciences.

[25]  Natalie L. M. Cappaert,et al.  The anatomy of memory: an interactive overview of the parahippocampal–hippocampal network , 2009, Nature Reviews Neuroscience.

[26]  L. Davachi,et al.  Category‐specificity in the human medial temporal lobe cortex , 2009, Hippocampus.

[27]  Christian F. Doeller,et al.  Evidence for grid cells in a human memory network , 2010, Nature.

[28]  Greg O. Horne,et al.  Controlling low-level image properties: The SHINE toolbox , 2010, Behavior research methods.

[29]  Lawrence L. Wald,et al.  Three dimensional echo-planar imaging at 7 Tesla , 2010, NeuroImage.

[30]  Richard N. Henson,et al.  Stimulus content and the neural correlates of source memory , 2011, Brain Research.

[31]  Arno Klein,et al.  A reproducible evaluation of ANTs similarity metric performance in brain image registration , 2011, NeuroImage.

[32]  Dwight J. Kravitz,et al.  A new neural framework for visuospatial processing , 2011, Nature Reviews Neuroscience.

[33]  Sachin S. Deshmukh,et al.  Representation of Non-Spatial and Spatial Information in the Lateral Entorhinal Cortex , 2011, Front. Behav. Neurosci..

[34]  B. Staresina,et al.  Perirhinal and Parahippocampal Cortices Differentially Contribute to Later Recollection of Object- and Scene-Related Event Details , 2011, The Journal of Neuroscience.

[35]  Nathaniel J. Killian,et al.  A map of visual space in the primate entorhinal cortex , 2012, Nature.

[36]  Abraham Z. Snyder,et al.  Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion , 2012, NeuroImage.

[37]  C. Ranganath,et al.  Two cortical systems for memory-guided behaviour , 2012, Nature Reviews Neuroscience.

[38]  C. Keysers,et al.  Probabilistic tractography recovers a rostrocaudal trajectory of connectivity variability in the human insular cortex , 2011, Human brain mapping.

[39]  Arne D. Ekstrom,et al.  Differential Connectivity of Perirhinal and Parahippocampal Cortices within Human Hippocampal Subregions Revealed by High-Resolution Functional Imaging , 2012, The Journal of Neuroscience.

[40]  J. Peters,et al.  Direct Evidence for Domain-Sensitive Functional Subregions in Human Entorhinal Cortex , 2012, The Journal of Neuroscience.

[41]  Craig E L Stark,et al.  Intrinsic functional connectivity of the human medial temporal lobe suggests a distinction between adjacent MTL cortices and hippocampus , 2012, Hippocampus.

[42]  Edward B. O'Neil,et al.  Distinct Familiarity-Based Response Patterns for Faces and Buildings in Perirhinal and Parahippocampal Cortex , 2013, The Journal of Neuroscience.

[43]  Fenna M. Krienen,et al.  Opportunities and limitations of intrinsic functional connectivity MRI , 2013, Nature Neuroscience.

[44]  Mark W. Woolrich,et al.  Resting-state fMRI in the Human Connectome Project , 2013, NeuroImage.

[45]  Essa Yacoub,et al.  The WU-Minn Human Connectome Project: An overview , 2013, NeuroImage.

[46]  Lila Davachi,et al.  Perirhinal-Hippocampal Connectivity during Reactivation Is a Marker for Object-Based Memory Consolidation , 2013, Neuron.

[47]  Edvard I. Moser,et al.  Grid Cells and Neural Coding in High-End Cortices , 2013, Neuron.

[48]  M. Moser,et al.  Traces of Experience in the Lateral Entorhinal Cortex , 2013, Current Biology.

[49]  David A. Boas,et al.  MRI parcellation of ex vivo medial temporal lobe , 2014, NeuroImage.

[50]  R. Mayeux,et al.  Molecular drivers and cortical spread of lateral entorhinal cortex dysfunction in preclinical Alzheimer's disease , 2013, Nature Neuroscience.

[51]  K. Schleifer,et al.  Targeted enhancement of cortical-hippocampal brain networks and associative memory , 2014 .

[52]  Sachin S. Deshmukh,et al.  Functional correlates of the lateral and medial entorhinal cortex: objects, path integration and local–global reference frames , 2014, Philosophical Transactions of the Royal Society B: Biological Sciences.

[53]  Zachariah M. Reagh,et al.  Object and spatial mnemonic interference differentially engage lateral and medial entorhinal cortex in humans , 2014, Proceedings of the National Academy of Sciences.

[54]  Ricardo Insausti,et al.  Identification of the human medial temporal lobe regions on magnetic resonance images , 2014, Human brain mapping.

[55]  Alberto Llera,et al.  ICA-AROMA: A robust ICA-based strategy for removing motion artifacts from fMRI data , 2015, NeuroImage.

[56]  C. Ranganath,et al.  Functional subregions of the human entorhinal cortex , 2015, eLife.

[57]  Jonathan D. Power,et al.  Recent progress and outstanding issues in motion correction in resting state fMRI , 2015, NeuroImage.

[58]  Rhodri Cusack,et al.  Automatic analysis (aa): efficient neuroimaging workflows and parallel processing using Matlab and XML , 2015, Front. Neuroinform..

[59]  Maarten Mennes,et al.  Evaluation of ICA-AROMA and alternative strategies for motion artifact removal in resting state fMRI , 2015, NeuroImage.