Routes to, from and within the subiculum

The subiculum is one of the major output areas of the hippocampus and has extensive projections to extrahippocampal targets. It is likely to play a pivotal role in the distribution of outgoing information from the hippocampus. The hippocampus, including the subiculum, is important for the formation, consolidation and retrieval of memory. These functions require a network that is flexible enough to encode incoming information and also allows for reliable distribution, storage and integration into previously encoded memories. Finally, relevant information has to be retrieved in a context-specific manner to allow for an appropriate behavioral response. The subiculum as a gateway between the hippocampus and cortex might serve to integrate and process information from the hippocampus proper and its other inputs before conveying it to more permanent storage locations. This review summarizes how the subiculum is embedded into upstream and downstream circuits, describes what is known about the local network topology and discusses cellular and functional properties of subicular cells subtypes. Lastly, it describes how these properties might help to separate information into parallel output streams and distribute it to its multiple target areas.

[1]  I. Soltesz,et al.  New dimensions of interneuronal specialization unmasked by principal cell heterogeneity , 2012, Trends in Neurosciences.

[2]  P. E. Sharp Subicular place cells generate the same “map” for different environments: Comparison with hippocampal cells , 2006, Behavioural Brain Research.

[3]  Yangfan Peng,et al.  Excitatory Microcircuits within Superficial Layers of the Medial Entorhinal Cortex. , 2017, Cell reports.

[4]  M. Wilson,et al.  Disruption of ripple‐associated hippocampal activity during rest impairs spatial learning in the rat , 2009, Hippocampus.

[5]  M. Schultzberg,et al.  Distribution of neuropeptide Y receptors in the rat hippocampal region , 1987, Neuroscience Letters.

[6]  N Spruston,et al.  Resting and active properties of pyramidal neurons in subiculum and CA1 of rat hippocampus. , 2000, Journal of neurophysiology.

[7]  M. Witter,et al.  Subicular efferents are organized mostly as parallel projections: A double‐labeling, retrograde‐tracing study in the rat , 1998, The Journal of comparative neurology.

[8]  Mark S. Cembrowski,et al.  Spatial Gene-Expression Gradients Underlie Prominent Heterogeneity of CA1 Pyramidal Neurons , 2016, Neuron.

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

[10]  Athanassios G. Siapas,et al.  Membrane Potential Dynamics of CA1 Pyramidal Neurons during Hippocampal Ripples in Awake Mice , 2016, Neuron.

[11]  D. Amaral,et al.  The three-dimensional organization of the hippocampal formation: A review of anatomical data , 1989, Neuroscience.

[12]  T. Dugladze,et al.  Cell Type-Specific Separation of Subicular Principal Neurons during Network Activities , 2015, PloS one.

[13]  R. Passingham The hippocampus as a cognitive map J. O'Keefe & L. Nadel, Oxford University Press, Oxford (1978). 570 pp., £25.00 , 1979, Neuroscience.

[14]  D. Schmitz,et al.  Differential cAMP Signaling at Hippocampal Output Synapses , 2008, The Journal of Neuroscience.

[15]  Dietmar Schmitz,et al.  Cellular and System Biology of Memory: Timing, Molecules, and Beyond. , 2016, Physiological reviews.

[16]  Menno P. Witter,et al.  Connections of the subiculum of the rat: Topography in relation to columnar and laminar organization , 2006, Behavioural Brain Research.

[17]  Attila Losonczy,et al.  Parvalbumin-Positive Basket Cells Differentiate among Hippocampal Pyramidal Cells , 2014, Neuron.

[18]  Masahiko Takada,et al.  Topographical organization of subicular neurons projecting to subcortical regions , 1994, Brain Research Bulletin.

[19]  G. Buzsáki,et al.  Selective suppression of hippocampal ripples impairs spatial memory , 2009, Nature Neuroscience.

[20]  Szabolcs Káli,et al.  Mechanisms of Sharp Wave Initiation and Ripple Generation , 2014, The Journal of Neuroscience.

[21]  L. Frank,et al.  Awake Hippocampal Sharp-Wave Ripples Support Spatial Memory , 2012, Science.

[22]  G. V. Hoesen,et al.  A direct projection from the perirhinal cortex (area 35) to the subiculum in the rat , 1983, Brain Research.

[23]  S. Sikdar,et al.  Depression biased non‐Hebbian spike‐timing‐dependent synaptic plasticity in the rat subiculum , 2014, The Journal of physiology.

[24]  S. O’Mara,et al.  Analysis of recordings of single-unit firing and population activity in the dorsal subiculum of unrestrained, freely moving rats. , 2003, Journal of neurophysiology.

[25]  Kat Christiansen,et al.  The subiculum: the heart of the extended hippocampal system. , 2015, Progress in brain research.

[26]  G. Shepherd,et al.  The neocortical circuit: themes and variations , 2015, Nature Neuroscience.

[27]  B. McNaughton,et al.  Reactivation of hippocampal ensemble memories during sleep. , 1994, Science.

[28]  Christian Wozny,et al.  Synaptic plasticity in the subiculum , 2009, Progress in Neurobiology.

[29]  Robert E Hampson,et al.  Differential but Complementary Mnemonic Functions of the Hippocampus and Subiculum , 2004, Neuron.

[30]  Xiangmin Xu,et al.  Noncanonical connections between the subiculum and hippocampal CA1 , 2016, The Journal of comparative neurology.

[31]  D. Amaral,et al.  Organization of CA1 projections to the subiculum: A PHA‐L analysis in the rat , 1991, Hippocampus.

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

[33]  Hippocampal pyramidal neurons comprise two distinct cell types that are countermodulated by metabotropic receptors. , 2012, Neuron.

[34]  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.

[35]  Yasuo Kawaguchi,et al.  Fast-spiking non-pyramidal cells in the hippocampal CA3 region, dentate gyrus and subiculum of rats , 1987, Brain Research.

[36]  Chen Sun,et al.  Distinct Neural Circuits for the Formation and Retrieval of Episodic Memories , 2017, Cell.

[37]  Sandro Romani,et al.  Hippocampal global remapping for different sensory modalities in flying bats , 2016, Nature Neuroscience.

[38]  Surya Ganguli,et al.  Behavioral/systems/cognitive Spatial Information Outflow from the Hippocampal Circuit: Distributed Spatial Coding and Phase Precession in the Subiculum , 2022 .

[39]  R. Yuste,et al.  Dense, Unspecific Connectivity of Neocortical Parvalbumin-Positive Interneurons: A Canonical Microcircuit for Inhibition? , 2011, The Journal of Neuroscience.

[40]  Yangfan Peng,et al.  Layer-Specific Organization of Local Excitatory and Inhibitory Synaptic Connectivity in the Rat Presubiculum , 2017, Cerebral cortex.

[41]  Mattias P. Karlsson,et al.  Awake replay of remote experiences in the hippocampus , 2009, Nature Neuroscience.

[42]  G. Buzsáki,et al.  Selective activation of deep layer (V-VI) retrohippocampal cortical neurons during hippocampal sharp waves in the behaving rat , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[43]  A. Ylinen,et al.  Reciprocal Connections between the Amygdala and the Hippocampal Formation, Perirhinal Cortex, and Postrhinal Cortex in Rat: A Review , 2000, Annals of the New York Academy of Sciences.

[44]  G. Buzsáki,et al.  High-Frequency Oscillations in the Output Networks of the Hippocampal–Entorhinal Axis of the Freely Behaving Rat , 1996, The Journal of Neuroscience.

[45]  D. Schmitz,et al.  Two different forms of long‐term potentiation at CA1–subiculum synapses , 2008, The Journal of physiology.

[46]  A. Mason,et al.  Neuronal diversity in the subiculum: correlations with the effects of somatostatin on intrinsic properties and on GABA-mediated IPSPs in vitro. , 1996, Journal of Neurophysiology.

[47]  S. Hestrin,et al.  Intracortical circuits of pyramidal neurons reflect their long-range axonal targets , 2009, Nature.

[48]  Albert K. Lee,et al.  Memory of Sequential Experience in the Hippocampus during Slow Wave Sleep , 2002, Neuron.

[49]  M. Wilson,et al.  Coordinated memory replay in the visual cortex and hippocampus during sleep , 2007, Nature Neuroscience.

[50]  F. H. Lopes da Silva,et al.  Networks of the Hippocampal Memory System of the Rat: The Pivotal Role of the Subiculum a , 2000, Annals of the New York Academy of Sciences.

[51]  M. Witter,et al.  Topographical and laminar organization of subicular projections to the parahippocampal region of the rat , 2003, The Journal of comparative neurology.

[52]  Yangfan Peng,et al.  Functional Diversity of Subicular Principal Cells during Hippocampal Ripples , 2015, The Journal of Neuroscience.

[53]  D. Schmitz,et al.  Group II Metabotropic Glutamate Receptors Depress Synaptic Transmission onto Subicular Burst Firing Neurons , 2012, PloS one.

[54]  M. Stewart Antidromic and orthodromic responses by subicular neurons in rat brain slices , 1997, Brain Research.

[55]  Douglas A. Nitz,et al.  Subiculum Neurons Map the Current Axis of Travel , 2016 .

[56]  N. Spruston,et al.  Action Potential Bursting in Subicular Pyramidal Neurons Is Driven by a Calcium Tail Current , 2001, The Journal of Neuroscience.

[57]  N. Spruston,et al.  Target‐specific output patterns are predicted by the distribution of regular‐spiking and bursting pyramidal neurons in the subiculum , 2012, Hippocampus.

[58]  Daniel Gomez-Dominguez,et al.  Determinants of different deep and superficial CA1 pyramidal cell dynamics during sharp-wave ripples , 2015, Nature Neuroscience.

[59]  J. Lisman Bursts as a unit of neural information: making unreliable synapses reliable , 1997, Trends in Neurosciences.

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

[61]  E. Callaway,et al.  Previously Published Works Uc Irvine Title: Cell-type-specific Circuit Connectivity of Hippocampal Ca1 Revealed through Cre-dependent Rabies Tracing Cell-type Specific Circuit Connectivity of Hippocampal Ca1 Revealed through Cre-dependent Rabies Tracing Nih Public Access Author Manuscript , 2022 .

[62]  D. Amaral,et al.  Entorhinal cortex of the monkey: V. Projections to the dentate gyrus, hippocampus, and subicular complex , 1991, The Journal of comparative neurology.

[63]  G. Buzsáki Two-stage model of memory trace formation: A role for “noisy” brain states , 1989, Neuroscience.

[64]  J. T. Erichsen,et al.  Parallel but separate inputs from limbic cortices to the mammillary bodies and anterior thalamic nuclei in the rat , 2010, The Journal of comparative neurology.

[65]  Song-Lin Ding,et al.  Comparative anatomy of the prosubiculum, subiculum, presubiculum, postsubiculum, and parasubiculum in human, monkey, and rodent , 2013, The Journal of comparative neurology.

[66]  M. Witter,et al.  Heterogeneity in the Dorsal Subiculum of the Rat. Distinct Neuronal Zones Project to Different Cortical and Subcortical Targets , 1990, The European journal of neuroscience.