Dynamics of place, boundary and object encoding in rat anterior claustrum

Discrete populations of brain cells signal differing types of spatial information. These “spatial cells” are largely confined to a closely-connected network of sites. We describe here, for the first time, cells in the anterior claustrum of the freely-moving rat encoding place, boundary and object information. This novel claustral spatial signal potentially directly modulates a wide variety of anterior cortical regions. We hypothesize that one of the functions of the claustrum is to provide information about body position, boundaries and landmark information, enabling dynamic control of behavior.

[1]  Morris Moscovitch,et al.  Preserved spatial memory after hippocampal lesions: effects of extensive experience in a complex environment , 2005, Nature Neuroscience.

[2]  M. Sadowski,et al.  Rat's claustrum shows two main cortico-related zones , 1997, Brain Research.

[3]  Beata Ludkiewicz,et al.  Qualitative and quantitative study of the postnatal development of the rabbit claustrum , 2002, International Journal of Developmental Neuroscience.

[4]  T. J. Teyler,et al.  Functional relations of the rodent claustral-entorhinal-hippocampal system , 1986, Brain Research.

[5]  Richard Reilly,et al.  Oscillatory entrainment of thalamic neurons by theta rhythm in freely moving rats. , 2011, Journal of neurophysiology.

[6]  C. Koch,et al.  What is the function of the claustrum? , 2005, Philosophical Transactions of the Royal Society B: Biological Sciences.

[7]  Vincent Hok,et al.  Behavioral / Systems / Cognitive Hippocampal Dynamics Predict Interindividual Cognitive Differences in Rats , 2012 .

[8]  R U Muller,et al.  Head-direction cells recorded from the postsubiculum in freely moving rats. I. Description and quantitative analysis , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[10]  Ian H. Stevenson,et al.  Spatially Distributed Local Fields in the Hippocampus Encode Rat Position , 2014, Science.

[11]  Juan Alvarez-Linera,et al.  The claustrum and its projection system in the human brain: a microsurgical and tractographic anatomical study. , 2008, Journal of neurosurgery.

[12]  Christoph Kayser,et al.  Unimodal Responses Prevail within the Multisensory Claustrum , 2010, The Journal of Neuroscience.

[13]  Lawrence Edelstein,et al.  Hypotheses relating to the function of the claustrum , 2012, Front. Integr. Neurosci..

[14]  S. Molden,et al.  Place fields of rat hippocampal pyramidal cells and spatial learning in the watermaze , 2001, The European journal of neuroscience.

[15]  Bruce L. McNaughton,et al.  An Information-Theoretic Approach to Deciphering the Hippocampal Code , 1992, NIPS.

[16]  G. Buzsáki,et al.  Memory, navigation and theta rhythm in the hippocampal-entorhinal system , 2013, Nature Neuroscience.

[17]  T. P. S. Powell,et al.  The organization of the connections between the cortex and the claustrum in the monkey , 1982, Brain Research.

[18]  J. O'Keefe,et al.  The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. , 1971, Brain research.

[19]  G. Buzsáki Theta rhythm of navigation: Link between path integration and landmark navigation, episodic and semantic memory , 2005, Hippocampus.

[20]  M. Moser,et al.  Representation of Geometric Borders in the Entorhinal Cortex , 2008, Science.

[21]  J. O’Keefe,et al.  Boundary Vector Cells in the Subiculum of the Hippocampal Formation , 2009, The Journal of Neuroscience.

[22]  Vincent Hok,et al.  Rosiglitazone enhances learning, place cell activity, and synaptic plasticity in middle-aged rats , 2012, Neurobiology of Aging.

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

[24]  Arthur W. Toga,et al.  Neural Networks of the Mouse Neocortex , 2014, Cell.

[25]  R. Muller,et al.  Attention-Like Modulation of Hippocampus Place Cell Discharge , 2010, The Journal of Neuroscience.

[26]  G. Paxinos,et al.  The Rat Brain in Stereotaxic Coordinates , 1983 .

[27]  Ariel Y Deutch,et al.  Proteomic analysis illuminates a novel structural definition of the claustrum and insula. , 2009, Cerebral cortex.

[28]  S. O’Mara,et al.  Responses of dorsal subicular neurons of rats during object exploration in an extended environment , 2004, Experimental Brain Research.

[29]  Howard Eichenbaum,et al.  A cognitive map for object memory in the hippocampus. , 2009, Learning & memory.

[30]  P. E. Sharp,et al.  Spatial correlates of firing patterns of single cells in the subiculum of the freely moving rat , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[31]  M. Moser,et al.  Optogenetic Dissection of Entorhinal-Hippocampal Functional Connectivity , 2013, Science.

[32]  May-Britt Moser,et al.  Mapping Your Every Move , 2014, Cerebrum : the Dana forum on brain science.

[33]  Y. Miyashita,et al.  Neural organization for the long-term memory of paired associates , 1991, Nature.

[34]  M. P. Witter,et al.  Reciprocal connections of the insular and piriform claustrum with limbic cortex: An anatomical study in the cat , 1988, Neuroscience.

[35]  Menno P. Witter,et al.  Place Cells and Place Recognition Maintained by Direct Entorhinal-Hippocampal Circuitry , 2002, Science.

[36]  J. Dziewia̧tkowski,et al.  The cortico-related zones of the rabbit claustrum—study of the claustrocortical connections based on the retrograde axonal transport of fluorescent tracers , 1998, Brain Research.

[37]  A. M. Graybiel,et al.  Sensory maps in the claustrum of the cat , 1980, Nature.

[38]  David C Rowland,et al.  Neural Correlates of Long-Term Object Memory in the Mouse Anterior Cingulate Cortex , 2012, The Journal of Neuroscience.

[39]  L. Edelstein,et al.  The claustrum: a historical review of its anatomy, physiology, cytochemistry and functional significance. , 2004, Cellular and molecular biology.

[40]  Mark P. Brandon,et al.  Segregation of cortical head direction cell assemblies on alternating theta cycles , 2013, Nature Neuroscience.

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

[42]  R. Muller,et al.  The firing of hippocampal place cells in the dark depends on the rat's recent experience , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[43]  R. Muller,et al.  The firing of hippocampal place cells predicts the future position of freely moving rats , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[44]  Charlotte N. Boccara,et al.  Grid cells in pre- and parasubiculum , 2010, Nature Neuroscience.

[45]  M. E. Corcoran,et al.  Susceptibility to Kindling and Neuronal Connections of the Anterior Claustrum , 2001, The Journal of Neuroscience.

[46]  Asla Pitkänen,et al.  Projections from the amygdaloid complex to the claustrum and the endopiriform nucleus: A Phaseolus vulgaris leucoagglutinin study in the rat , 2002, The Journal of comparative neurology.

[47]  J Tanji,et al.  Neuronal activity in the claustrum of the monkey during performance of multiple movements. , 1996, Journal of neurophysiology.

[48]  Christoph Kayser,et al.  A role of the claustrum in auditory scene analysis by reflecting sensory change , 2014, Front. Syst. Neurosci..

[49]  E. Save,et al.  Flexible use of proximal objects and distal cues by hippocampal place cells , 2007, Hippocampus.

[50]  Kevin D. Alloway,et al.  Rat Claustrum Coordinates But Does Not Integrate Somatosensory and Motor Cortical Information , 2012, The Journal of Neuroscience.

[51]  J. T. Erichsen,et al.  Theta-Modulated Head Direction Cells in the Rat Anterior Thalamus , 2011, The Journal of Neuroscience.

[52]  Soyoung Q. Park,et al.  The Claustrum and Insula in Microcebus murinus: A High Resolution Diffusion Imaging Study , 2012, Front. Neuroanat..

[53]  M. E. Corcoran,et al.  Kindling of claustrum and insular cortex: comparison to perirhinal cortex in the rat , 2001, The European journal of neuroscience.

[54]  B. McNaughton,et al.  Theta phase precession in hippocampal neuronal populations and the compression of temporal sequences , 1996, Hippocampus.

[55]  C A Barnes,et al.  Representation of three‐dimensional objects by the rat perirhinal cortex , 2012, Hippocampus.

[56]  K M Gothard,et al.  Binding of hippocampal CA1 neural activity to multiple reference frames in a landmark-based navigation task , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[57]  J. T. Erichsen,et al.  Nucleus reuniens of the thalamus contains head direction cells , 2014, eLife.

[58]  R. Muller,et al.  The effects of changes in the environment on the spatial firing of hippocampal complex-spike cells , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[59]  Bruno Cozzi,et al.  Topography of Gng2- and NetrinG2-Expression Suggests an Insular Origin of the Human Claustrum , 2012, PloS one.

[60]  L. Swanson The Rat Brain in Stereotaxic Coordinates, George Paxinos, Charles Watson (Eds.). Academic Press, San Diego, CA (1982), vii + 153, $35.00, ISBN: 0 125 47620 5 , 1984 .

[61]  M. Moser,et al.  Pattern Separation in the Dentate Gyrus and CA3 of the Hippocampus , 2007, Science.

[62]  Jean-Pierre Timmermans,et al.  Differentiation in the immunocytochemical features of intrinsic and cortically projecting neurons in the rat claustrum — combined immunocytochemical and axonal transport study , 2001, Brain Research.

[63]  J. T. Erichsen,et al.  Hippocampal–anterior thalamic pathways for memory: uncovering a network of direct and indirect actions , 2010, The European journal of neuroscience.

[64]  Y. Naya,et al.  Integrating What and When Across the Primate Medial Temporal Lobe , 2011, Science.

[65]  Brian N. Mathur,et al.  The claustrum in review , 2014, Front. Syst. Neurosci..

[66]  J. T. Erichsen,et al.  The anterior thalamus provides a subcortical circuit supporting memory and spatial navigation , 2013, Front. Syst. Neurosci..

[67]  Jeffrey Taube,et al.  Head direction cells , 2009, Scholarpedia.

[68]  J. Dziewia̧tkowski,et al.  Comparative Anatomy of the Claustrum in Selected Species: A Morphometric Analysis , 1998, Brain, Behavior and Evolution.

[69]  K. Grasby,et al.  The anterior claustrum and spatial reversal learning in rats , 2013, Brain Research.

[70]  David C Rowland,et al.  Neural correlates of novel object and novel location recognition behavior in the mouse anterior cingulate cortex. , 2009, Journal of neurophysiology.