Retrosplenial Cortex Indexes Stability beyond the Spatial Domain

Retrosplenial cortex (RSC) is highly responsive to landmarks in the environment that remain fixed in a permanent location, and this has been linked with its known involvement in scene and spatial processing. However, it is unclear whether RSC representations of permanence are a purely spatial phenomenon or whether they extend into behavioral and conceptual domains. To test this, during functional MRI scanning, we had people (males and females) read three different types of sentences that described either something permanent or transient. The first two sentence types were imageable, with a focus either on a spatial landmark or on an action. The third type of sentence involved non-imageable abstract concepts. We found that, in addition to being more active for sentences describing landmarks with a permanent location in space, RSC was also significantly engaged by sentences describing stable and consistent behaviors or actions, as long as they were rooted within a concrete imageable setting. RSC was not responsive to abstract concepts, even those that embodied the notion of stability. Similarly, it was not engaged by imageable sentences with transient contents. In contrast, parahippocampal cortex was more engaged by imageable sentences describing landmarks, whereas the hippocampus was active for all imageable sentences. In addition, for imageable sentences describing permanence, there was bidirectional functional coupling between RSC and these medial temporal lobe structures. It appears, therefore, that RSC-mediated permanence representations could be helpful for more than spatially mapping environments and may also provide information about the reliability of events occurring within them. SIGNIFICANCE STATEMENT The retrosplenial cortex (RSC) is known to process information about landmarks in the environment that have a fixed, permanent location. Here we tested whether this permanence response was apparent beyond the spatial domain, which could have implications for understanding the role of the RSC more widely across cognition. We found that the RSC was engaged not only by permanent landmarks but also by stable and consistent actions. It was not responsive to transient landmarks or actions or to abstract concepts, even those that embodied the notion of stability. We conclude that the RSC might do more than help to map spatial environments, by possibly also providing information about the reliability of events occurring within them.

[1]  Marvin M Chun,et al.  Eye movements help link different views in scene-selective cortex. , 2011, Cerebral cortex.

[2]  Eleanor A. Maguire,et al.  Efficacy of navigation may be influenced by retrosplenial cortex-mediated learning of landmark stability , 2017, Neuropsychologia.

[3]  Karl J. Friston The free-energy principle: a unified brain theory? , 2010, Nature Reviews Neuroscience.

[4]  D. Amaral,et al.  Macaque monkey retrosplenial cortex: III. Cortical efferents , 2003, The Journal of comparative neurology.

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

[6]  Daniel D. Dilks,et al.  Mirror-Image Sensitivity and Invariance in Object and Scene Processing Pathways , 2011, The Journal of Neuroscience.

[7]  D. Amaral,et al.  Macaque monkey retrosplenial cortex: II. Cortical afferents , 2003, The Journal of comparative neurology.

[8]  M. Petrides,et al.  Retrosplenial and hippocampal brain regions in human navigation: complementary functional contributions to the formation and use of cognitive maps , 2007, The European journal of neuroscience.

[9]  E. Maguire Deconstructing episodic memory with , 2007 .

[10]  Karl J. Friston,et al.  Stochastic dynamic causal modelling of fMRI data: Should we care about neural noise? , 2012, NeuroImage.

[11]  Peter Zeidman,et al.  A central role for the retrosplenial cortex in de novo environmental learning , 2015, eLife.

[12]  Sterling C. Johnson,et al.  A generalized form of context-dependent psychophysiological interactions (gPPI): A comparison to standard approaches , 2012, NeuroImage.

[13]  J M Wyss,et al.  Connections of the retrosplenial dysgranular cortex in the rat , 1992, The Journal of comparative neurology.

[14]  Soojin Park,et al.  Different roles of the parahippocampal place area (PPA) and retrosplenial cortex (RSC) in panoramic scene perception , 2009, NeuroImage.

[15]  Bruce L. McNaughton,et al.  Sparse orthogonal population representation of spatial context in the retrosplenial cortex , 2017, Nature Communications.

[16]  Kate Jeffery,et al.  An independent, landmark-dominated head direction signal in dysgranular retrosplenial cortex , 2016, Nature Neuroscience.

[17]  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.

[18]  S. Becker,et al.  Remembering the past and imagining the future: a neural model of spatial memory and imagery. , 2007, Psychological review.

[19]  S. Shinkareva,et al.  Neural representation of abstract and concrete concepts: A meta‐analysis of neuroimaging studies , 2010, Human brain mapping.

[20]  Karl J. Friston,et al.  Dynamic causal modelling , 2003, NeuroImage.

[21]  Alain Berthoz,et al.  Multiple reference frames used by the human brain for spatial perception and memory , 2010, Experimental Brain Research.

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

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

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

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

[26]  Demis Hassabis,et al.  The construction system of the brain , 2009, Philosophical Transactions of the Royal Society B: Biological Sciences.

[27]  T. van Groen,et al.  Connections of the retrosplenial granular a cortex in the rat , 1990, The Journal of comparative neurology.

[28]  T. van Groen,et al.  Connections of the retrosplenial granular b cortex in the rat , 1990, The Journal of comparative neurology.

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

[30]  Dwight J. Kravitz,et al.  Real-World Scene Representations in High-Level Visual Cortex: It's the Spaces More Than the Places , 2011, The Journal of Neuroscience.

[31]  Adam M. P. Miller,et al.  Retrosplenial Cortical Neurons Encode Navigational Cues, Trajectories and Reward Locations During Goal Directed Navigation , 2016, Cerebral cortex.

[32]  Eleanor A. Maguire,et al.  Assessing the mechanism of response in the retrosplenial cortex of good and poor navigators☆ , 2013, Cortex.

[33]  Anna L. Powell,et al.  The rat retrosplenial cortex as a link for frontal functions: A lesion analysis , 2017, Behavioural Brain Research.

[34]  Karl J. Friston,et al.  Bayesian model selection for group studies , 2009, NeuroImage.

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

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

[37]  Yaoda Xu,et al.  The Role of Transverse Occipital Sulcus in Scene Perception and Its Relationship to Object Individuation in Inferior Intraparietal Sulcus , 2013, Journal of Cognitive Neuroscience.

[38]  A. Roepstorff,et al.  Concrete spatial language: See what I mean? , 2005, Brain and Language.

[39]  Roger B. H. Tootell,et al.  Spatial encoding and underlying circuitry in scene-selective cortex , 2013, NeuroImage.

[40]  K Friston,et al.  Stochastic Dynamic Causal Modelling , 2009, NeuroImage.

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

[42]  E. Maguire,et al.  Anterior hippocampus: the anatomy of perception, imagination and episodic memory , 2016, Nature Reviews Neuroscience.

[43]  J. Aggleton,et al.  The rat retrosplenial cortex is required when visual cues are used flexibly to determine location , 2014, Behavioural Brain Research.

[44]  Russell A. Epstein,et al.  Anchoring the neural compass: Coding of local spatial reference frames in human medial parietal lobe , 2014, Nature Neuroscience.

[45]  A. Alexander,et al.  Spatially Periodic Activation Patterns of Retrosplenial Cortex Encode Route Sub-spaces and Distance Traveled , 2017, Current Biology.

[46]  Leslie G. Ungerleider,et al.  Scene-Selective Cortical Regions in Human and Nonhuman Primates , 2011, The Journal of Neuroscience.

[47]  Adam Kilgarriff,et al.  Putting frequencies in the dictionary , 1997 .

[48]  Mary Hegarty,et al.  The Human Retrosplenial Cortex and Thalamus Code Head Direction in a Global Reference Frame , 2016, The Journal of Neuroscience.