Assessing the mechanism of response in the retrosplenial cortex of good and poor navigators☆

The retrosplenial cortex (RSC) is consistently engaged by a range of tasks that examine episodic memory, imagining the future, spatial navigation, and scene processing. Despite this, an account of its exact contribution to these cognitive functions remains elusive. Here, using functional MRI (fMRI) and multi-voxel pattern analysis (MVPA) we found that the RSC coded for the specific number of permanent outdoor items that were in view, that is, items which are fixed and never change their location. Moreover, this effect was selective, and was not apparent for other item features such as size and visual salience. This detailed detection of the number of permanent items in view was echoed in the parahippocampal cortex (PHC), although the two brain structures diverged when participants were divided into good and poor navigators. There was no difference in the responsivity of the PHC between the two groups, while significantly better decoding of the number of permanent items in view was possible from patterns of activity in the RSC of good compared to poor navigators. Within good navigators, the RSC also facilitated significantly better prediction of item permanence than the PHC. Overall, these findings suggest that the RSC in particular is concerned with coding the presence of every permanent item that is in view. This mechanism may represent a key building block for spatial and scene representations that are central to episodic memories and imagining the future, and could also be a prerequisite for successful navigation.

[1]  Shigeo Abe DrEng Pattern Classification , 2001, Springer London.

[2]  P. E. Sharp,et al.  Head direction, place, and movement correlates for cells in the rat retrosplenial cortex. , 2001, Behavioral neuroscience.

[3]  Jeffrey S. Taube,et al.  Origins of landmark encoding in the brain , 2011, Trends in Neurosciences.

[4]  David G. Stork,et al.  Pattern Classification , 1973 .

[5]  John P. Aggleton,et al.  Understanding retrosplenial amnesia: Insights from animal studies , 2010, Neuropsychologia.

[6]  Isabelle Guyon,et al.  An Introduction to Variable and Feature Selection , 2003, J. Mach. Learn. Res..

[7]  D. Hassabis,et al.  Deconstructing episodic memory with construction , 2007, Trends in Cognitive Sciences.

[8]  N. Foster,et al.  Metabolic reduction in the posterior cingulate cortex in very early Alzheimer's disease , 1997, Annals of neurology.

[9]  D. Hassabis,et al.  Decoding Neuronal Ensembles in the Human Hippocampus , 2009, Current Biology.

[10]  Russell A. Epstein Cognitive Neuroscience: Scene Layout from Vision and Touch , 2011, Current Biology.

[11]  Chih-Jen Lin,et al.  A comparison of methods for multiclass support vector machines , 2002, IEEE Trans. Neural Networks.

[12]  Demis Hassabis,et al.  Decoding overlapping memories in the medial temporal lobes using high-resolution fMRI , 2011, Learning & memory.

[13]  J R Hodges,et al.  Retrosplenial cortex (BA 29/30) hypometabolism in mild cognitive impairment (prodromal Alzheimer's disease) , 2003, The European journal of neuroscience.

[14]  D. Hassabis,et al.  Decoding Individual Episodic Memory Traces in the Human Hippocampus , 2010, Current Biology.

[15]  A. Siegel,et al.  The development of spatial representations of large-scale environments. , 1975, Advances in child development and behavior.

[16]  A. Oliva,et al.  A familiar-size Stroop effect: real-world size is an automatic property of object representation. , 2012, Journal of experimental psychology. Human perception and performance.

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

[18]  Russell A. Epstein,et al.  Multiple object properties drive scene-selective regions. , 2014, Cerebral cortex.

[19]  H. Duvernoy,et al.  The Human Brain: Surface, Three-Dimensional Sectional Anatomy with MRI, and Blood Supply , 1999 .

[20]  Sean M. Polyn,et al.  Beyond mind-reading: multi-voxel pattern analysis of fMRI data , 2006, Trends in Cognitive Sciences.

[21]  M. Bar Visual objects in context , 2004, Nature Reviews Neuroscience.

[22]  Sharon L. Thompson-Schill,et al.  Learning Places from Views: Variation in Scene Processing as a Function of Experience and Navigational Ability , 2005, Journal of Cognitive Neuroscience.

[23]  John O. Willis,et al.  Wechsler Abbreviated Scale of Intelligence , 2014 .

[24]  Eleanor A. Maguire,et al.  Retrosplenial Cortex Codes for Permanent Landmarks , 2012, PloS one.

[25]  J. Hodges,et al.  Focal posterior cingulate atrophy in incipient Alzheimer's disease , 2010, Neurobiology of Aging.

[26]  Gabriele Janzen,et al.  Memory consolidation of landmarks in good navigators , 2008, Hippocampus.

[27]  Gabriele Janzen,et al.  Neural Encoding of Objects Relevant for Navigation and Resting State Correlations with Navigational Ability , 2011, Journal of Cognitive Neuroscience.

[28]  Mohammad Dastjerdi,et al.  Neural populations in human posteromedial cortex display opposing responses during memory and numerical processing , 2012, Proceedings of the National Academy of Sciences.

[29]  D. Hassabis,et al.  Using Imagination to Understand the Neural Basis of Episodic Memory , 2007, The Journal of Neuroscience.

[30]  Eleanor A. Maguire,et al.  Decoding information in the human hippocampus: A user's guide , 2012, Neuropsychologia.

[31]  R Turner,et al.  Optimisation of the 3D MDEFT sequence for anatomical brain imaging: technical implications at 1.5 and 3 T , 2004, NeuroImage.

[32]  Alana T. Wong,et al.  Remembering the past and imagining the future: Common and distinct neural substrates during event construction and elaboration , 2007, Neuropsychologia.

[33]  David C. Zhu,et al.  Full Scenes produce more activation than Close-up Scenes and Scene-Diagnostic Objects in parahippocampal and retrosplenial cortex: An fMRI study , 2008, Brain and Cognition.

[34]  J. Baron,et al.  Relationships between Hippocampal Atrophy, White Matter Disruption, and Gray Matter Hypometabolism in Alzheimer's Disease , 2008, The Journal of Neuroscience.

[35]  E. Maguire,et al.  What does the retrosplenial cortex do? , 2009, Nature Reviews Neuroscience.

[36]  Rainer Goebel,et al.  Information-based functional brain mapping. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[37]  Russell A. Epstein Parahippocampal and retrosplenial contributions to human spatial navigation , 2008, Trends in Cognitive Sciences.

[38]  John M. Henderson,et al.  Functions of parahippocampal place area and retrosplenial cortex in real-world scene analysis: An fMRI study , 2011 .

[39]  R. N. Spreng,et al.  The Future of Memory: Remembering, Imagining, and the Brain , 2012, Neuron.

[40]  W. K. Simmons,et al.  Circular analysis in systems neuroscience: the dangers of double dipping , 2009, Nature Neuroscience.

[41]  B. Levine,et al.  The functional neuroanatomy of autobiographical memory: A meta-analysis , 2006, Neuropsychologia.

[42]  R. Nathan Spreng,et al.  The Common Neural Basis of Autobiographical Memory, Prospection, Navigation, Theory of Mind, and the Default Mode: A Quantitative Meta-analysis , 2009, Journal of Cognitive Neuroscience.

[43]  Chih-Jen Lin,et al.  LIBSVM: A library for support vector machines , 2011, TIST.

[44]  Russell A. Epstein,et al.  Constructing scenes from objects in human occipitotemporal cortex , 2011, Nature Neuroscience.

[45]  Dwight J. Kravitz,et al.  Deconstructing visual scenes in cortex: gradients of object and spatial layout information. , 2013, Cerebral cortex.

[46]  P. Perona,et al.  Rapid natural scene categorization in the near absence of attention , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[47]  Eleanor A Maguire,et al.  A New Role for the Parahippocampal Cortex in Representing Space , 2011, The Journal of Neuroscience.

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

[49]  Nikolaus Weiskopf,et al.  Decoding Representations of Scenes in the Medial Temporal Lobes , 2011, Hippocampus.

[50]  E A Maguire,et al.  Neuroimaging studies of autobiographical event memory. , 2001, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[51]  Anthony E. Richardson,et al.  Development of a self-report measure of environmental spatial ability. , 2002 .

[52]  E. Maguire,et al.  Newcastle University Eprints , 2022 .

[53]  Nikolaus Weiskopf,et al.  Optimal EPI parameters for reduction of susceptibility-induced BOLD sensitivity losses: A whole-brain analysis at 3 T and 1.5 T , 2006, NeuroImage.

[54]  E. J. Green,et al.  Head-direction cells in the rat posterior cortex , 1994, Experimental Brain Research.

[55]  Emily J. Ward,et al.  How reliable are visual context effects in the parahippocampal place area? , 2010, Cerebral cortex.

[56]  Karl J. Friston,et al.  Unified segmentation , 2005, NeuroImage.

[57]  J. Haynes Brain Reading: Decoding Mental States From Brain Activity In Humans , 2011 .

[58]  Karl J. Friston,et al.  Voxel-Based Morphometry—The Methods , 2000, NeuroImage.

[59]  E. Maguire The retrosplenial contribution to human navigation: a review of lesion and neuroimaging findings. , 2001, Scandinavian journal of psychology.