Cholinergic modulation of spatial learning, memory and navigation

Spatial learning, including encoding and retrieval of spatial memories as well as holding spatial information in working memory generally serving navigation under a broad range of circumstances, relies on a network of structures. While central to this network are medial temporal lobe structures with a widely appreciated crucial function of the hippocampus, neocortical areas such as the posterior parietal cortex and the retrosplenial cortex also play essential roles. Since the hippocampus receives its main subcortical input from the medial septum of the basal forebrain (BF) cholinergic system, it is not surprising that the potential role of the septo‐hippocampal pathway in spatial navigation has been investigated in many studies. Much less is known of the involvement in spatial cognition of the parallel projection system linking the posterior BF with neocortical areas. Here we review the current state of the art of the division of labour within this complex ‘navigation system’, with special focus on how subcortical cholinergic inputs may regulate various aspects of spatial learning, memory and navigation.

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

[2]  N. Urban,et al.  Layer- and cell type-selective co-transmission by a basal forebrain cholinergic projection to the olfactory bulb , 2017, Nature Communications.

[3]  T. Steckler,et al.  Effects of NBM lesions with two neurotoxins on spatial memory and autoshaping , 1993, Pharmacology Biochemistry and Behavior.

[4]  B. Hangya,et al.  Monitoring the Right Collection: The Central Cholinergic Neurons as an Instructive Example , 2017, Front. Neural Circuits.

[5]  D. Brown,et al.  Muscarinic Acetylcholine Receptors (mAChRs) in the Nervous System: Some Functions and Mechanisms , 2010, Journal of Molecular Neuroscience.

[6]  T. Freund,et al.  Innervation of different peptide-containing neurons in the hippocampus by gabaergic septal afferents , 1990, Neuroscience.

[7]  Anna Maria Di Betta,et al.  Retrograde amnesia in a patient with retrosplenial tumour , 1998 .

[8]  Mark P. Brandon,et al.  Reduction of Theta Rhythm Dissociates Grid Cell Spatial Periodicity from Directional Tuning , 2011, Science.

[9]  T. Gould,et al.  The effects of acute nicotine, chronic nicotine, and withdrawal from chronic nicotine on performance of a cued appetitive response. , 2013, Behavioral neuroscience.

[10]  Edvard I. Moser,et al.  Speed cells in the medial entorhinal cortex , 2015, Nature.

[11]  R. Burke,et al.  The relative selectivity of anticholinergic drugs for the M1 and M2 muscarinic receptor subtypes , 1986, Movement disorders : official journal of the Movement Disorder Society.

[12]  A. Nordberg Human nicotinic receptors—Their role in aging and dementia , 1994, Neurochemistry International.

[13]  Heping Cheng,et al.  Fast high-resolution miniature two-photon microscopy for brain imaging in freely behaving mice , 2017, Nature Methods.

[14]  L. Savage,et al.  Blunted hippocampal, but not striatal, acetylcholine efflux parallels learning impairment in diencephalic-lesioned rats , 2007, Neurobiology of Learning and Memory.

[15]  J. Pearce,et al.  The effect of retrosplenial cortex lesions in rats on incidental and active spatial learning , 2015, Front. Behav. Neurosci..

[16]  D. S. Olton,et al.  Intrahippocampal grafts of fetal basal forebrain tissue alter place fields in the hippocampus of rats with fimbria-fornix lesions , 1989, Neuroscience.

[17]  G. Akopian,et al.  Striatal Direct and Indirect Pathway Output Structures Are Differentially Altered in Mouse Models of Huntington's Disease , 2018, The Journal of Neuroscience.

[18]  A. Nuñez,et al.  Modulation of hippocampal theta oscillations and spatial memory by relaxin-3 neurons of the nucleus incertus. , 2009, Learning & memory.

[19]  M. Hasselmo The role of acetylcholine in learning and memory , 2006, Current Opinion in Neurobiology.

[20]  Bernardo L. Sabatini,et al.  Mechanisms and functions of GABA co-release , 2016, Nature Reviews Neuroscience.

[21]  A. Gamal,et al.  Miniaturized integration of a fluorescence microscope , 2011, Nature Methods.

[22]  Attila Losonczy,et al.  Sublayer-Specific Coding Dynamics during Spatial Navigation and Learning in Hippocampal Area CA1 , 2016, Neuron.

[23]  Alexander M. Herman,et al.  A cholinergic basal forebrain feeding circuit modulates appetite suppression , 2016, Nature.

[24]  M. Bear,et al.  A Cholinergic Mechanism for Reward Timing within Primary Visual Cortex , 2013, Neuron.

[25]  D. R. Montello,et al.  Spatial knowledge acquisition from direct experience in the environment: Individual differences in the development of metric knowledge and the integration of separately learned places , 2006, Cognitive Psychology.

[26]  Jeffrey L. Krichmar,et al.  A Computational Model for Spatial Navigation Based on Reference Frames in the Hippocampus, Retrosplenial Cortex, and Posterior Parietal Cortex , 2017, Front. Neurorobot..

[27]  E. Vizi,et al.  Neurochemistry and pharmacology of the major hippocampal transmitter systems: Synaptic and nonsynaptic interactions , 1998, Hippocampus.

[28]  F. Gage,et al.  Choice behavior of rats searching for food , 1977 .

[29]  Brian E. Russ,et al.  The Basal Forebrain Regulates Global Resting-State fMRI Fluctuations , 2018, Neuron.

[30]  Eleanor A. Maguire,et al.  Thoughts, behaviour, and brain dynamics during navigation in the real world , 2006, NeuroImage.

[31]  Michael E. Hasselmo,et al.  Modeling goal-directed spatial navigation in the rat based on physiological data from the hippocampal formation , 2003, Neural Networks.

[32]  L. Acsády,et al.  Calretinin is present in non-pyramidal cells of the rat hippocampus—III. Their inputs from the median raphe and medial septal nuclei , 1993, Neuroscience.

[33]  Nathan G. Clack,et al.  Vibrissa-Based Object Localization in Head-Fixed Mice , 2010, The Journal of Neuroscience.

[34]  J. Hagan,et al.  Blockade of spatial learning by the M1 muscarinic antagonist pirenzepine , 2004, Psychopharmacology.

[35]  C. Shute,et al.  The cholinergic limbic system: projections to hippocampal formation, medial cortex, nuclei of the ascending cholinergic reticular system, and the subfornical organ and supra-optic crest. , 1967, Brain : a journal of neurology.

[36]  Fuqiang Xu,et al.  Whole-Brain Monosynaptic Afferent Inputs to Basal Forebrain Cholinergic System , 2016, Front. Neuroanat..

[37]  Bruno Poucet,et al.  Involvement of the hippocampus and associative parietal cortex in the use of proximal and distal landmarks for navigation , 2000, Behavioural Brain Research.

[38]  Asohan Amarasingham,et al.  Hippocampus Internally Generated Cell Assembly Sequences in the Rat , 2011 .

[39]  Shanguang Chen,et al.  Chronic scopolamine-injection-induced cognitive deficit on reward-directed instrumental learning in rat is associated with CREB signaling activity in the cerebral cortex and dorsal hippocampus , 2013, Psychopharmacology.

[40]  S. Allen,et al.  Coexistence of choline acetyltransferase and nerve growth factor receptors in the rat basal forebrain , 1988, Neuroscience Letters.

[41]  E. Albuquerque,et al.  The nicotinic acetylcholine receptor subtypes and their function in the hippocampus and cerebral cortex. , 2004, Progress in brain research.

[42]  L. Nadel,et al.  Viewpoints: how the hippocampus contributes to memory, navigation and cognition , 2017, Nature Neuroscience.

[43]  R. Clark,et al.  The Hippocampus and Spatial Memory: Findings with a Novel Modification of the Water Maze , 2007, The Journal of Neuroscience.

[44]  A. Gonzalo-Ruiz,et al.  Localization of amino acids, neuropeptides and cholinergic markers in neurons of the septum-diagonal band complex projecting to the retrosplenial granular cortex of the rat , 2000, Brain Research Bulletin.

[45]  J. Pilcher,et al.  Scopolamine Impairs Spatial Working Memory in the Radial Maze:An Analysis by Error Type and Arm Choice1 , 1997, Pharmacology Biochemistry and Behavior.

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

[47]  A. Ekstrom,et al.  Close but no cigar: Spatial precision deficits following medial temporal lobe lesions provide novel insight into theoretical models of navigation and memory , 2018, Hippocampus.

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

[49]  F. J. Staay,et al.  The T-maze continuous alternation task for assessing the effects of putative cognition enhancers in the mouse , 2004, Behavioural Brain Research.

[50]  Armin Brandt,et al.  Neural Activity in Human Hippocampal Formation Reveals the Spatial Context of Retrieved Memories , 2013, Science.

[51]  Kazuto Kobayashi,et al.  Distinct roles of basal forebrain cholinergic neurons in spatial and object recognition memory , 2015, Scientific Reports.

[52]  M. Gallagher,et al.  Ageing: the cholinergic hypothesis of cognitive decline , 1995, Current Opinion in Neurobiology.

[53]  B. J. Clark,et al.  Interaction of Egocentric and World-Centered Reference Frames in the Rat Posterior Parietal Cortex , 2014, The Journal of Neuroscience.

[54]  L. Jarrard,et al.  Effects of medial and lateral septal lesions on acquisition of a place and cue radial maze task , 1992, Behavioural Brain Research.

[55]  S. Arneric,et al.  Effects of ABT-418, a novel cholinergic channel ligand, on place learning in septal-lesioned rats. , 1994, European journal of pharmacology.

[56]  M. Baxter,et al.  Effects of complete immunotoxin lesions of the cholinergic basal forebrain on fear conditioning and spatial learning , 2004, Hippocampus.

[57]  M. Hasselmo,et al.  Potential roles of cholinergic modulation in the neural coding of location and movement speed , 2016, Journal of Physiology-Paris.

[58]  N. Burgess,et al.  The hippocampus is required for short‐term topographical memory in humans , 2007, Hippocampus.

[59]  M. Mesulam,et al.  The cholinergic system in the pathophysiology and treatment of Alzheimer's disease. , 2018, Brain : a journal of neurology.

[60]  Paul E. Gold,et al.  Patterns of brain acetylcholine release predict individual differences in preferred learning strategies in rats , 2003, Neurobiology of Learning and Memory.

[61]  Morris Moscovitch,et al.  Mental space travel: damage to posterior parietal cortex prevents egocentric navigation and reexperiencing of remote spatial memories. , 2010, Journal of experimental psychology. Learning, memory, and cognition.

[62]  Gerit Pfuhl,et al.  Functional Split between Parietal and Entorhinal Cortices in the Rat , 2012, Neuron.

[63]  J. Yakel Nicotinic ACh receptors in the hippocampus: role in excitability and plasticity. , 2012, Nicotine & tobacco research : official journal of the Society for Research on Nicotine and Tobacco.

[64]  J. Gorry STUDIES ON THE COMPARATIVE ANATOMY OF THE GANGLION BASALE OF MEYNERT. , 1963, Acta anatomica.

[65]  A. Kirkwood,et al.  Neuromodulators Control the Polarity of Spike-Timing-Dependent Synaptic Plasticity , 2007, Neuron.

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

[67]  B T Hyman,et al.  H. M.’s Medial Temporal Lobe Lesion: Findings from Magnetic Resonance Imaging , 1997, The Journal of Neuroscience.

[68]  Morris Moscovitch,et al.  An investigation of the effects of hippocampal lesions in rats on pre‐ and postoperatively acquired spatial memory in a complex environment , 2010, Hippocampus.

[69]  H. Mansvelder,et al.  Cholinergic Modulation of Cortical Microcircuits Is Layer-Specific: Evidence from Rodent, Monkey and Human Brain , 2017, Front. Neural Circuits.

[70]  A. Arnsten,et al.  Nicotinic α4β2 Cholinergic Receptor Influences on Dorsolateral Prefrontal Cortical Neuronal Firing during a Working Memory Task , 2017, The Journal of Neuroscience.

[71]  F. Joseph McClernon,et al.  Nicotinic effects on cognitive function: behavioral characterization, pharmacological specification, and anatomic localization , 2006, Psychopharmacology.

[72]  E K Perry,et al.  Correlation of cholinergic abnormalities with senile plaques and mental test scores in senile dementia. , 1978, British medical journal.

[73]  Tristan D. McClure-Begley,et al.  Faculty Opinions recommendation of Dopaminergic neurons inhibit striatal output through non-canonical release of GABA. , 2012 .

[74]  Ashesh K Dhawale,et al.  Automated long-term recording and analysis of neural activity in behaving animals , 2016, bioRxiv.

[75]  Arne D. Ekstrom,et al.  Impairments in precision, rather than spatial strategy, characterize performance on the virtual Morris Water Maze: A case study , 2016, Neuropsychologia.

[76]  G. Buzsáki,et al.  The cholinergic nucleus basalis: a key structure in neocortical arousal. , 1989, EXS.

[77]  Peter Somogyi,et al.  Synaptic Targets of Medial Septal Projections in the Hippocampus and Extrahippocampal Cortices of the Mouse , 2015, The Journal of Neuroscience.

[78]  M. Gallagher,et al.  Thalamic and basal forebrain cholinergic connections of the rat posterior parietal cortex. , 1999, Neuroreport.

[79]  P. Haydon,et al.  Septal Cholinergic Neuromodulation Tunes the Astrocyte-Dependent Gating of Hippocampal NMDA Receptors to Wakefulness , 2017, Neuron.

[80]  F. Fadda,et al.  Increased hippocampal acetylcholine release during a working memory task. , 1996, European journal of pharmacology.

[81]  D M Bowen,et al.  Neurotransmitter-related enzymes and indices of hypoxia in senile dementia and other abiotrophies. , 1976, Brain : a journal of neurology.

[82]  G. Buzsáki,et al.  Optogenetic activation of septal cholinergic neurons suppresses sharp wave ripples and enhances theta oscillations in the hippocampus , 2014, Proceedings of the National Academy of Sciences.

[83]  J. Taube The head direction signal: origins and sensory-motor integration. , 2007, Annual review of neuroscience.

[84]  A. Berthoz,et al.  Reference Frames for Spatial Cognition: Different Brain Areas are Involved in Viewer-, Object-, and Landmark-Centered Judgments About Object Location , 2004, Journal of Cognitive Neuroscience.

[85]  R. J. McDonald,et al.  Multiple Parallel Memory Systems in the Brain of the Rat , 2002, Neurobiology of Learning and Memory.

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

[87]  J. Fadel,et al.  Cholinergic regulation of fear learning and extinction , 2017, Journal of neuroscience research.

[88]  R. Andersen,et al.  Posterior parietal cortex. , 1989, Reviews of oculomotor research.

[89]  Ehren L. Newman,et al.  Precise spike timing dynamics of hippocampal place cell activity sensitive to cholinergic disruption , 2017, Hippocampus.

[90]  Ritchie E. Brown,et al.  Cholinergic Neurons Excite Cortically Projecting Basal Forebrain GABAergic Neurons , 2014, The Journal of Neuroscience.

[91]  C. Schreiner,et al.  A synaptic memory trace for cortical receptive field plasticity , 2007, Nature.

[92]  Weikun Guo,et al.  Astrocytic adenosine receptor A2A and Gs-coupled signaling regulate memory , 2014, Nature Neuroscience.

[93]  Francesca Sargolini,et al.  Independence of landmark and self-motion-guided navigation: a different role for grid cells , 2014, Philosophical Transactions of the Royal Society B: Biological Sciences.

[94]  R. Gaykema,et al.  Cortical projection patterns of the medial septum‐diagonal band complex , 1990, The Journal of comparative neurology.

[95]  N. Burgess,et al.  Lost and found: bespoke memory testing for Alzheimer's disease and semantic dementia. , 2010, Journal of Alzheimer's disease : JAD.

[96]  Minmin Luo,et al.  Hypothalamic Circuits for Predation and Evasion , 2018, Neuron.

[97]  A. Levey,et al.  Cholinergic innervation of cortex by the basal forebrain: Cytochemistry and cortical connections of the septal area, diagonal band nuclei, nucleus basalis (Substantia innominata), and hypothalamus in the rhesus monkey , 1983, The Journal of comparative neurology.

[98]  Matthew A Wilson,et al.  Enhancement of encoding and retrieval functions through theta phase-specific manipulation of hippocampus , 2014, eLife.

[99]  R. Wiley,et al.  Specificity of 192 IgG-saporin for NGF receptor-positive cholinergic basal forebrain neurons in the rat , 1992, Brain Research.

[100]  T. Freund,et al.  Types and synaptic connections of hippocampal inhibitory neurons reciprocally connected with the medial septum , 2008, The European journal of neuroscience.

[101]  W. Low,et al.  Cholinergic innervation of the retrosplenial cortex via the fornix pathway as determined by high affinity choline uptake, choline acetyltransferase activity, and muscarinic receptor binding in the rat , 1994, Neurochemical Research.

[102]  David A. Johnson,et al.  Recognition of novel objects and their location in rats with selective cholinergic lesion of the medial septum , 2012, Neuroscience Letters.

[103]  Joshua I. Sanders,et al.  Cortical interneurons that specialize in disinhibitory control , 2013, Nature.

[104]  L. Záborszky,et al.  Organization of ascending hypothalamic projections to the rostral forebrain with special reference to the innervation of cholinergic projection neurons , 1991, The Journal of comparative neurology.

[105]  L. Acsády,et al.  Medial septal and median raphe innervation of vasoactive intestinal polypeptide-containing interneurons in the hippocampus , 1999, Neuroscience.

[106]  R. Muller,et al.  The Effects on Place Cells of Local Scopolamine Dialysis Are Mimicked by a Mixture of Two Specific Muscarinic Antagonists , 2004, The Journal of Neuroscience.

[107]  P. Somogyi,et al.  Enrichment of cholinergic synaptic terminals on GABAergic neurons and coexistence of immunoreactive GABA and choline acetyltransferase in the same synaptic terminals in the striate cortex of the cat , 1991, The Journal of comparative neurology.

[108]  E. Levin,et al.  Acute and chronic nicotine effects on working memory in aged rats , 2005, Psychopharmacology.

[109]  Russell A. Epstein,et al.  Human entorhinal cortex represents visual space using a boundary-anchored grid , 2017, Nature Neuroscience.

[110]  C. Pfeffer,et al.  Inhibitory Neurons: Vip Cells Hit the Brake on Inhibition , 2014, Current Biology.

[111]  Hongkui Zeng,et al.  Generation of a whole-brain atlas for the cholinergic system and mesoscopic projectome analysis of basal forebrain cholinergic neurons , 2017, Proceedings of the National Academy of Sciences.

[112]  Cody A. Siciliano,et al.  α6β2 subunit containing nicotinic acetylcholine receptors exert opposing actions on rapid dopamine signaling in the nucleus accumbens of rats with high-versus low-response to novelty , 2017, Neuropharmacology.

[113]  Brad E. Pfeiffer,et al.  Hippocampal place cell sequences depict future paths to remembered goals , 2013, Nature.

[114]  Arjan Blokland,et al.  The validity of scopolamine as a pharmacological model for cognitive impairment: A review of animal behavioral studies , 2010, Neuroscience & Biobehavioral Reviews.

[115]  Dmitriy Aronov,et al.  Mapping of a non-spatial dimension by the hippocampal/entorhinal circuit , 2017, Nature.

[116]  T. Freund,et al.  Co-transmission of acetylcholine and GABA regulates hippocampal states , 2018, Nature Communications.

[117]  E. Maguire,et al.  Navigation around London by a taxi driver with bilateral hippocampal lesions. , 2006, Brain : a journal of neurology.

[118]  J. Sirviö,et al.  Effects of concurrent manipulations of nicotinic and muscarinic receptors on spatial and passive avoidance learning , 1990, Pharmacology Biochemistry and Behavior.

[119]  J. Feigenbaum,et al.  Allocentric versus egocentric spatial memory after unilateral temporal lobectomy in humans. , 2004, Neuropsychology.

[120]  Jeffrey S. Taube,et al.  Impaired Head Direction Cell Representation in the Anterodorsal Thalamus after Lesions of the Retrosplenial Cortex , 2010, The Journal of Neuroscience.

[121]  Minmin Luo,et al.  Habenula “Cholinergic” Neurons Corelease Glutamate and Acetylcholine and Activate Postsynaptic Neurons via Distinct Transmission Modes , 2011, Neuron.

[122]  Carey Y. L. Huh,et al.  Glutamatergic Neurons of the Mouse Medial Septum and Diagonal Band of Broca Synaptically Drive Hippocampal Pyramidal Cells: Relevance for Hippocampal Theta Rhythm , 2010, The Journal of Neuroscience.

[123]  C. Barry,et al.  Task Demands Predict a Dynamic Switch in the Content of Awake Hippocampal Replay , 2017, Neuron.

[124]  Liqun Luo,et al.  Circuit Architecture of VTA Dopamine Neurons Revealed by Systematic Input-Output Mapping , 2015, Cell.

[125]  L. Mucke,et al.  Spatial cognition and the human navigation network in AD and MCI , 2007, Neurology.

[126]  Jerome S. Cohen,et al.  Response perseveration in the hippocampal lesioned rat , 1971 .

[127]  T. Yaguchi,et al.  Dilinoleoylphosphatidylcholine ameliorates scopolamine-induced impairment of spatial learning and memory by targeting alpha7 nicotinic ACh receptors. , 2009, Life sciences.

[128]  R. Wiley,et al.  The behavioral functions of the cholinergic basalforebrain : lessons from 192 IgG-SAPORIN , 1998, International Journal of Developmental Neuroscience.

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

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

[131]  Flavia Filimon,et al.  Are All Spatial Reference Frames Egocentric? Reinterpreting Evidence for Allocentric, Object-Centered, or World-Centered Reference Frames , 2015, Front. Hum. Neurosci..

[132]  Z. Gu,et al.  Cholinergic Coordination of Presynaptic and Postsynaptic Activity Induces Timing-Dependent Hippocampal Synaptic Plasticity , 2012, The Journal of Neuroscience.

[133]  Antoine Adamantidis,et al.  Causal evidence for the role of REM sleep theta rhythm in contextual memory consolidation , 2016, Science.

[134]  J. Yakel,et al.  Desensitization of nicotinic ACh receptors: shaping cholinergic signaling , 2005, Trends in Neurosciences.

[135]  C. H. Honzik,et al.  Degrees of hunger, reward and non-reward, and maze learning in rats, and Introduction and removal of reward, and maze performance in rats , 1930 .

[136]  Christian Büchel,et al.  Neural foundations of emerging route knowledge in complex spatial environments. , 2004, Brain research. Cognitive brain research.

[137]  E. Tolman Cognitive maps in rats and men. , 1948, Psychological review.

[138]  Thomas J. Wills,et al.  Reconciling the different faces of hippocampal theta: The role of theta oscillations in cognitive, emotional and innate behaviors , 2018, Neuroscience & Biobehavioral Reviews.

[139]  M. Gallagher,et al.  Selective immunotoxic lesions of basal forebrain cholinergic cells: effects on learning and memory in rats. , 1995, Behavioral neuroscience.

[140]  Ehren L. Newman,et al.  Grid cell spatial tuning reduced following systemic muscarinic receptor blockade , 2014, Hippocampus.

[141]  G. Weniger,et al.  Egocentric memory impaired and allocentric memory intact as assessed by virtual reality in subjects with unilateral parietal cortex lesions , 2009, Neuropsychologia.

[142]  David J. Foster,et al.  Memory and Space: Towards an Understanding of the Cognitive Map , 2015, The Journal of Neuroscience.

[143]  T Hope,et al.  Getting Lost in Dementia: A Longitudinal Study of a Behavioral Symptom , 1998, International Psychogeriatrics.

[144]  M. Danik,et al.  A functional glutamatergic neurone network in the medial septum and diagonal band area , 2005, The Journal of physiology.

[145]  I. Gritti,et al.  Stereological estimates of the basal forebrain cell population in the rat, including neurons containing choline acetyltransferase, glutamic acid decarboxylase or phosphate-activated glutaminase and colocalizing vesicular glutamate transporters , 2006, Neuroscience.

[146]  M. Baxter,et al.  Cholinergic modulation of a specific memory function of prefrontal cortex , 2011, Nature Neuroscience.

[147]  S. Lacalle,et al.  Cell loss and nuclear hypertrophy in topographical subdivisions of the nucleus basalis of Meynert in Alzheimer's disease , 1991, Neuroscience.

[148]  Anna L. Powell,et al.  What does spatial alternation tell us about retrosplenial cortex function? , 2015, Front. Behav. Neurosci..

[149]  Z. Henderson,et al.  The projection from the striatum to the nucleus basalis in the rat: an electron microscopic study , 1997, Neuroscience.

[150]  Karim Benchenane,et al.  Explicit memory creation during sleep demonstrates a causal role of place cells in navigation , 2015, Nature Neuroscience.

[151]  Caroline A. Johnson,et al.  A direct GABAergic output from the basal ganglia to frontal cortex , 2014, Nature.

[152]  Michael Frotscher,et al.  Cholinergic innervation of the rat hippocampus as revealed by choline acetyltransferase immunocytochemistry: A combined light and electron microscopic study , 1985, The Journal of comparative neurology.

[153]  T. Arendt,et al.  The cholinergic system in aging and neuronal degeneration , 2011, Behavioural Brain Research.

[154]  B. Sabatini,et al.  Corelease of acetylcholine and GABA from cholinergic forebrain neurons , 2015, eLife.

[155]  R. Wiley,et al.  Immunolesioning: selective destruction of neurons using immunotoxin to rat NGF receptor , 1991, Brain Research.

[156]  M. Andermann,et al.  Imaging Neuronal Populations in Behaving Rodents: Paradigms for Studying Neural Circuits Underlying Behavior in the Mammalian Cortex , 2013, The Journal of Neuroscience.

[157]  T. Freund,et al.  GABAergic interneurons containing calbindin D28K or somatostatin are major targets of GABAergic basal forebrain afferents in the rat neocortex , 1991, The Journal of comparative neurology.

[158]  F. LaFerla,et al.  Amyloid-β expression in retrosplenial cortex of triple transgenic mice: relationship to cholinergic axonal afferents from medial septum , 2009, Neuroscience.

[159]  C. Nyakas,et al.  Detailed projection patterns of septal and diagonal band efferents to the hippocampus in the rat with emphasis on innervation of CA1 and dentate gyrus , 1987, Brain Research Bulletin.

[160]  L. Barbieri,et al.  Characterization of a Saponaria officinalis seed ribosome-inactivating protein: immunoreactivity and sequence homologies. , 1985, Biochemical and biophysical research communications.

[161]  T. Freund,et al.  Synaptic co-transmission of acetylcholine and GABA regulates hippocampal states , 2017, bioRxiv.

[162]  Anne E Carpenter,et al.  Neuron-type specific signals for reward and punishment in the ventral tegmental area , 2011, Nature.

[163]  Anna S. Mitchell,et al.  Retrosplenial Cortical Contributions to Anterograde and Retrograde Memory in the Monkey , 2016, Cerebral cortex.

[164]  Michael D. Adoff,et al.  The effects of acute, chronic, and withdrawal from chronic nicotine on novel and spatial object recognition in male C57BL/6J mice , 2011, Psychopharmacology.

[165]  R. Morris Spatial Localization Does Not Require the Presence of Local Cues , 1981 .

[166]  Guillén Fernández,et al.  Interaction between the Human Hippocampus and the Caudate Nucleus during Route Recognition , 2004, Neuron.

[167]  A. Chiba,et al.  Learning‐dependent dynamics of beta‐frequency oscillations in the basal forebrain of rats , 2010, The European journal of neuroscience.

[168]  I. Gritti,et al.  GABAergic and other noncholinergic basal forebrain neurons, together with cholinergic neurons, project to the mesocortex and isocortex in the rat , 1997, The Journal of comparative neurology.

[169]  D. Nitz Tracking Route Progression in the Posterior Parietal Cortex , 2006, Neuron.

[170]  York Winter,et al.  Spatial cognition in a virtual reality home-cage extension for freely moving rodents. , 2017, Journal of neurophysiology.

[171]  J. J. Chrobak,et al.  Timing of administration mediates the memory effects of intraseptal carbachol infusion , 2004, Neuroscience.

[172]  B. K. Hartman,et al.  Ultrastructural and morphometric features of the acetylcholine innervation in adult rat parietal cortex: An electron microscopic study in serial sections , 1994, The Journal of comparative neurology.

[173]  S. McKenzie,et al.  Hippocampus-dependent spatial learning is associated with higher global cognition among healthy older adults , 2017, Neuropsychologia.

[174]  T. Arendt,et al.  Immunofluorescence and immunoelectron microscopic evidence for differences in myelination of GABAergic and cholinergic septohippocampal fibres , 2001, International Journal of Developmental Neuroscience.

[175]  E. Andriambeloson,et al.  Methyllycaconitine- and scopolamine-induced cognitive dysfunction: differential reversal effect by cognition-enhancing drugs , 2014, Pharmacology research & perspectives.

[176]  P. E. Gold,et al.  Acetylcholine release in the hippocampus and striatum during place and response training. , 2005, Learning & memory.

[177]  Adam M. P. Miller,et al.  Cues, context, and long-term memory: the role of the retrosplenial cortex in spatial cognition , 2014, Front. Hum. Neurosci..

[178]  R. Morris,et al.  Place navigation impaired in rats with hippocampal lesions , 1982, Nature.

[179]  C. Petersen,et al.  Cholinergic signals in mouse barrel cortex during active whisker sensing. , 2014, Cell reports.

[180]  C. Qin,et al.  Neurochemical Phenotypes of the Afferent and Efferent Projections of the Mouse Medial Habenula Article in Press , 2022 .

[181]  D. Tank,et al.  Intracellular dynamics of hippocampal place cells during virtual navigation , 2009, Nature.

[182]  Jonathan W. Kelly,et al.  Optimal combination of environmental cues and path integration during navigation , 2018, Memory & cognition.

[183]  P. R. Hof,et al.  Comparative analysis of the nucleus basalis of Meynert among primates , 2011, Neuroscience.

[184]  Andrew P Maurer,et al.  Movement Enhances the Nonlinearity of Hippocampal Theta , 2016, The Journal of Neuroscience.

[185]  Richard S. J. Frackowiak,et al.  Knowing where and getting there: a human navigation network. , 1998, Science.

[186]  Z. Nadasdy,et al.  Neurons in the basal forebrain project to the cortex in a complex topographic organization that reflects corticocortical connectivity patterns: an experimental study based on retrograde tracing and 3D reconstruction. , 2015, Cerebral cortex.

[187]  P. Newhouse,et al.  Nicotine Treatment of Mild Cognitive Impairment: a 6-Month Double-Blind Pilot Clinical Trial , 2012, Neurology.

[188]  Karl Deisseroth,et al.  Astrocyte Intermediaries of Septal Cholinergic Modulation in the Hippocampus , 2016, Neuron.

[189]  Susumu Tonegawa,et al.  Conjunctive input processing drives feature selectivity in hippocampal CA1 neurons , 2015, Nature Neuroscience.

[190]  L. Acsády,et al.  Structural basis of the cholinergic and serotonergic modulation of GABAergic neurons in the hippocampus , 1999, Neurochemistry International.

[191]  A. Björklund,et al.  Behaviour-dependent changes in acetylcholine release in normal and graft-reinnervated hippocampus: Evidence for host regulation of grafted cholinergic neurons , 1992, Neuroscience.

[192]  R. McCarley,et al.  Cholinergic Neurons in the Basal Forebrain Promote Wakefulness by Actions on Neighboring Non-Cholinergic Neurons: An Opto-Dialysis Study , 2016, The Journal of Neuroscience.

[193]  G. Higgins,et al.  A double dissociation between serial reaction time and radial maze performance in rats subjected to 192 IgG‐saporin lesions of the nucleus basalis and/or the septal region , 2003, The European journal of neuroscience.

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

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

[196]  M. Baxter,et al.  Selective Immunolesions of Cholinergic Neurons in Mice: Effects on Neuroanatomy, Neurochemistry, and Behavior , 2001, The Journal of Neuroscience.

[197]  F. Roberts,et al.  The effect of pirenzepine on spatial learning in the Morris Water Maze , 1988, Pharmacology Biochemistry and Behavior.

[198]  B. Bontempi,et al.  Cognitive Enhancing Properties and Tolerability of Cholinergic Agents in Mice: A Comparative Study of Nicotine, Donepezil, and SIB-1553A, a Subtype-Selective Ligand for Nicotinic Acetylcholine Receptors , 2003, Neuropsychopharmacology.

[199]  L. Mucke,et al.  Network abnormalities and interneuron dysfunction in Alzheimer disease , 2016, Nature Reviews Neuroscience.

[200]  J. Brioni,et al.  Effect of intraventricular injections of dihydro-beta-erythroidine (DH,β E) on spatial memory in the rat , 1996, Brain Research.

[201]  H. Fukuyama,et al.  Directional Disorientation Following Left Retrosplenial Hemorrhage: a Case Report with FMRI Studies , 2007, Cortex.

[202]  James G. Heys,et al.  The Functional Micro-organization of Grid Cells Revealed by Cellular-Resolution Imaging , 2014, Neuron.

[203]  F. Fadda,et al.  Hippocampal acetylcholine release correlates with spatial learning performance in freely moving rats , 2000, Neuroreport.

[204]  Howard Eichenbaum,et al.  Cholinergic system regulation of spatial representation by the hippocampus , 2002, Hippocampus.

[205]  W. Scoville,et al.  LOSS OF RECENT MEMORY AFTER BILATERAL HIPPOCAMPAL LESIONS , 1957, Journal of neurology, neurosurgery, and psychiatry.

[206]  M. Mesulam,et al.  Central cholinergic pathways in the rat: An overview based on an alternative nomenclature (Ch1–Ch6) , 1983, Neuroscience.

[207]  J. Gray,et al.  Behavioural, histological and immunocytochemical consequences following 192 IgG-saporin immunolesions of the basal forebrain cholinergic system , 2001, Brain Research Bulletin.

[208]  永福 智志 The Organization of Learning , 2005, Journal of Cognitive Neuroscience.

[209]  M. Mesulam,et al.  Cortical projections arising from the basal forebrain: A study of cholinergic and noncholinergic components employing combined retrograde tracing and immunohistochemical localization of choline acetyltransferase , 1984, Neuroscience.

[210]  C. Geula,et al.  Cortical cholinergic fibers in aging and Alzheimer's disease: A morphometric study , 1989, Neuroscience.

[211]  A. Björklund,et al.  Selective Lesioning of the Basal Forebrain Cholinergic System by Intraventricular 192 IgG–saporin: Behavioural, Biochemical and Stereological Studies in the Rat , 1995, The European journal of neuroscience.

[212]  Z. Borhegyi,et al.  Parvalbumin-containing cells of the angular portion of the vertical limb terminate on calbindin-immunoreactive neurons located at the border between the lateral and medial septum of the rat , 2006, Experimental Brain Research.

[213]  A. Treves,et al.  Hippocampal remapping and grid realignment in entorhinal cortex , 2007, Nature.

[214]  E. Save,et al.  Medial entorhinal cortex and medial septum contribute to self-motion-based linear distance estimation , 2017, Brain Structure and Function.

[215]  Z. Gu,et al.  Timing-Dependent Septal Cholinergic Induction of Dynamic Hippocampal Synaptic Plasticity , 2011, Neuron.

[216]  A. Oliva,et al.  Distributed Representation of “What” and “Where” Information in the Parahippocampal Region , 2016, The Journal of Neuroscience.

[217]  J. Harding,et al.  The role of the AT4 and cholinergic systems in the Nucleus Basalis Magnocellularis (NBM): Effects on spatial memory , 2009, Brain Research.

[218]  B. Lambolez,et al.  Nicotinic Transmission onto Layer 6 Cortical Neurons Relies on Synaptic Activation of Non-α7 Receptors. , 2016, Cerebral cortex.

[219]  Alcino J. Silva,et al.  Encoding and storage of spatial information in the retrosplenial cortex , 2014, Proceedings of the National Academy of Sciences.

[220]  Kaori Takehara-Nishiuchi,et al.  Cholinergic Modulation of Frontoparietal Cortical Network Dynamics Supporting Supramodal Attention , 2018, The Journal of Neuroscience.

[221]  D. Price,et al.  Alzheimer disease: Plaques, tangles, and the basal forebrain , 1982, Annals of neurology.

[222]  R. Kesner,et al.  The Effects of Muscarinic Cholinergic Receptor Blockade in the Rat Anterior Cingulate and Prelimbic/Infralimbic Cortices on Spatial Working Memory , 1998, Neurobiology of Learning and Memory.

[223]  Etienne Save,et al.  The retrosplenial cortex is necessary for path integration in the dark , 2014, Behavioural Brain Research.

[224]  Tobias Navarro Schröder,et al.  Hexadirectional coding of visual space in human entorhinal cortex , 2018, Nature Neuroscience.

[225]  J. Aggleton Multiple anatomical systems embedded within the primate medial temporal lobe: Implications for hippocampal function , 2012, Neuroscience & Biobehavioral Reviews.

[226]  Neil Burgess,et al.  Hippocampal Volume Reduction in Humans Predicts Impaired Allocentric Spatial Memory in Virtual-Reality Navigation , 2015, The Journal of Neuroscience.

[227]  J. D. Bruin,et al.  Cholinergic receptor blockade in prefrontal cortex and lesions of the nucleus basalis: implications for allocentric and egocentric spatial memory in rats , 2002, Behavioural Brain Research.

[228]  Balázs Hangya,et al.  Open Source Tools for Temporally Controlled Rodent Behavior Suitable for Electrophysiology and Optogenetic Manipulations , 2018, Front. Syst. Neurosci..

[229]  M. T. Shipley,et al.  Cholinergic Inputs from Basal Forebrain Add an Excitatory Bias to Odor Coding in the Olfactory Bulb , 2014, The Journal of Neuroscience.

[230]  Asohan Amarasingham,et al.  Internally Generated Cell Assembly Sequences in the Rat Hippocampus , 2008, Science.

[231]  M. Petrides,et al.  Cognitive Strategies Dependent on the Hippocampus and Caudate Nucleus in Human Navigation: Variability and Change with Practice , 2003, The Journal of Neuroscience.

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

[233]  Ines Blockx,et al.  Cholinergic and serotonergic modulations differentially affect large-scale functional networks in the mouse brain , 2016, Brain Structure and Function.

[234]  Tobias Meilinger,et al.  Putting Egocentric and Allocentric into Perspective , 2010, Spatial Cognition.

[235]  A. Arnsten,et al.  Nicotinic α7 receptors enhance NMDA cognitive circuits in dorsolateral prefrontal cortex , 2013, Proceedings of the National Academy of Sciences.

[236]  M. Moser,et al.  A prefrontal–thalamo–hippocampal circuit for goal-directed spatial navigation , 2015, Nature.

[237]  B. Winters,et al.  Nicotinic receptor activation in perirhinal cortex and hippocampus enhances object memory in rats , 2012, Neuropharmacology.

[238]  Liqun Luo,et al.  Viral-genetic tracing of the input–output organization of a central norepinephrine circuit , 2015, Nature.

[239]  Ryan P. Vetreno,et al.  Impaired, spared, and enhanced ACh efflux across the hippocampus and striatum in diencephalic amnesia is dependent on task demands , 2008, Neurobiology of Learning and Memory.

[240]  Dmitriy Aronov,et al.  Engagement of Neural Circuits Underlying 2D Spatial Navigation in a Rodent Virtual Reality System , 2014, Neuron.

[241]  J. Yakel,et al.  Heteromeric α7β2 Nicotinic Acetylcholine Receptors in the Brain. , 2016, Trends in pharmacological sciences.

[242]  E. Levin,et al.  Nicotinic, muscarinic and dopaminergic actions in the ventral hippocampus and the nucleus accumbens: effects on spatial working memory in rats , 1996, Brain Research.

[243]  Richard B. Reilly,et al.  Medial septum regulates the hippocampal spatial representation , 2015, Front. Behav. Neurosci..

[244]  G. M. Peterson,et al.  Morphological evidence for a substance P projection from medial septum to hippocampus , 1992, Peptides.

[245]  B. Everitt,et al.  AMPA‐induced Lesions of the Basal Forebrain Differentially Affect Cholinergic and Non‐cholinergic Neurons: Lesion Assessment Using Quantitative In Situ Hybridization Histochemistry , 1995, The European journal of neuroscience.

[246]  M. Hasselmo,et al.  Modes and Models of Forebrain Cholinergic Neuromodulation of Cognition , 2011, Neuropsychopharmacology.

[247]  B. Vogt,et al.  Acetylcholine efflux from retrosplenial areas and hippocampal sectors during maze exploration , 2009, Behavioural Brain Research.

[248]  B. Hangya,et al.  Distinct behavioural and network correlates of two interneuron types in prefrontal cortex , 2013, Nature.

[249]  Michael J. Goard,et al.  Fast Modulation of Visual Perception by Basal Forebrain Cholinergic Neurons , 2013, Nature Neuroscience.

[250]  Simona Sava,et al.  Activation of the Medial Septum Reverses Age-Related Hippocampal Encoding Deficits: A Place Field Analysis , 2008, The Journal of Neuroscience.

[251]  L. Angelucci,et al.  Effects of concomitant nicotinic and muscarinic blockade on spatial memory disturbance in rats are purely additive: Evidence from the morris water task , 1994, Physiology & Behavior.

[252]  Jack Waters,et al.  Acetylcholine excites neocortical pyramidal neurons via nicotinic receptors. , 2015, Journal of neurophysiology.

[253]  B. Hangya,et al.  Central Cholinergic Neurons Are Rapidly Recruited by Reinforcement Feedback , 2015, Cell.

[254]  R. Morris,et al.  Place navigation in rats is impaired by lesions of medial septum and diagonal band but not nucleus basalis magnocellularis , 1988, Behavioural Brain Research.

[255]  Hanspeter A Mallot,et al.  Route Navigating without Place Recognition: What is Recognised in Recognition-Triggered Responses? , 2000, Perception.

[256]  R. Robertson,et al.  Basal forebrain and anterior thalamic contributions to acetylcholinesterase activity in granular retrosplenial cortex of rats , 1992, Brain Research.

[257]  Ashley N. Linder,et al.  The Spatial Periodicity of Grid Cells Is Not Sustained During Reduced Theta Oscillations , 2011, Science.

[258]  Jonathan W. Kelly,et al.  Cue combination in human spatial navigation , 2017, Cognitive Psychology.

[259]  Jean Gotman,et al.  Low-frequency theta oscillations in the human hippocampus during real-world and virtual navigation , 2017, Nature Communications.

[260]  E. Levin,et al.  Intracerebroventricular nicotine and mecamylamine alter radial‐arm maze performance in rats , 1994 .

[261]  Kenneth D Harris,et al.  Decision and navigation in mouse parietal cortex , 2017, bioRxiv.

[262]  Hao Wang,et al.  Different effects of scopolamine on the retrieval of spatial memory and fear memory , 2011, Behavioural Brain Research.

[263]  Roberta L. Klatzky,et al.  Allocentric and Egocentric Spatial Representations: Definitions, Distinctions, and Interconnections , 1998, Spatial Cognition.

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

[265]  T. Freund,et al.  GABA-containing neurons in the septum control inhibitory interneurons in the hippocampus , 1988, Nature.

[266]  David A. Johnson,et al.  Selective lesion of septal cholinergic neurons in rats impairs acquisition of a delayed matching to position T-maze task by delaying the shift from a response to a place strategy , 2008, Brain Research Bulletin.

[267]  T. Itakura,et al.  Neuropsychological deficits associated with a tumour in the posterior corpus callosum: A report of two cases , 2006, Brain injury.

[268]  Laszlo Zaborszky,et al.  Chapter 28 – The Basal Forebrain Cholinergic Projection System in Mice , 2012 .

[269]  R. Servatius,et al.  Medial Septum-Diagonal Band of Broca (MSDB) GABAergic Regulation of Hippocampal Acetylcholine Efflux Is Dependent on Cognitive Demands , 2014, The Journal of Neuroscience.

[270]  Larry R Squire,et al.  Impaired remote spatial memory after hippocampal lesions despite extensive training beginning early in life , 2005, Hippocampus.

[271]  Russell A. Epstein,et al.  The cognitive map in humans: spatial navigation and beyond , 2017, Nature Neuroscience.

[272]  Bruce L. McNaughton,et al.  Laminar organization of encoding and memory reactivation in the parietal cortex , 2017 .

[273]  D. Amaral,et al.  Hippocampal‐neocortical interaction: A hierarchy of associativity , 2000, Hippocampus.

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

[275]  R. McCarley,et al.  The menagerie of the basal forebrain: how many (neural) species are there, what do they look like, how do they behave and who talks to whom? , 2017, Current Opinion in Neurobiology.

[276]  B. McNaughton,et al.  Preserved spatial coding in hippocampal CA1 pyramidal cells during reversible suppression of CA3c output: evidence for pattern completion in hippocampus , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[277]  E. Levin,et al.  Dorsal hippocampal α7 and α4β2 nicotinic receptors and memory , 2006, Brain Research.

[278]  Adam Johnson,et al.  Triple Dissociation of Information Processing in Dorsal Striatum, Ventral Striatum, and Hippocampus on a Learned Spatial Decision Task , 2010, Neuron.

[279]  Martin Sarter,et al.  Behavioral-cognitive targets for cholinergic enhancement , 2015, Current Opinion in Behavioral Sciences.

[280]  A. Fisher,et al.  Reversal of age-related cognitive impairments by an M1 cholinergic agonist, AF102B , 1990, Pharmacology Biochemistry and Behavior.

[281]  G. Westbrook,et al.  Dual-transmitter neurons: functional implications of co-release and co-transmission , 2014, Current Opinion in Neurobiology.

[282]  G. Buzsáki,et al.  Hippocampal theta activity following selective lesion of the septal cholinergic systeM , 1994, Neuroscience.

[283]  André Dufour,et al.  Spatial navigation in normal aging and the prodromal stage of Alzheimer's disease: Insights from imaging and behavioral studies , 2013, Ageing Research Reviews.

[284]  A. Björklund,et al.  Acetylcholine release in the rat hippocampus as studied by microdialysis is dependent on axonal impulse flow and increases during behavioural activation , 1990, Neuroscience.

[285]  G. Fishell,et al.  A disinhibitory circuit mediates motor integration in the somatosensory cortex , 2013, Nature Neuroscience.

[286]  Hiroshi Moriwaki,et al.  Memory impairment and spatial disorientation following a left retrosplenial lesion , 2001, Journal of Clinical Neuroscience.

[287]  J. J. Chrobak,et al.  Intraseptal infusion of the cholinergic agonist carbachol impairs delayed‐non‐match‐to‐sample radial arm maze performance in the rat , 2004, Hippocampus.

[288]  B. Cosquer,et al.  Septohippocampal pathways contribute to system consolidation of a spatial memory: Sequential implication of gabaergic and cholinergic neurons , 2011, Hippocampus.

[289]  Li Jiang,et al.  Cholinergic Signaling Controls Conditioned Fear Behaviors and Enhances Plasticity of Cortical-Amygdala Circuits , 2016, Neuron.

[290]  C. Büchel,et al.  Dissociable Retrosplenial and Hippocampal Contributions to Successful Formation of Survey Representations , 2005, The Journal of Neuroscience.

[291]  Xiaojie Gao,et al.  Theta oscillations regulate the speed of locomotion via a hippocampus to lateral septum pathway , 2015, Nature Communications.

[292]  Z. Borhegyi,et al.  Phase Segregation of Medial Septal GABAergic Neurons during Hippocampal Theta Activity , 2004, The Journal of Neuroscience.

[293]  P. Luiten,et al.  Cholinergic and GABAergic neurons in the rat medial septum express muscarinic acetylcholine receptors , 1994, Brain Research.

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

[295]  M. Pai,et al.  Topographical disorientation in community‐residing patients with Alzheimer's disease , 2004, International journal of geriatric psychiatry.

[296]  D. Dupret,et al.  Hippocampal Offline Reactivation Consolidates Recently Formed Cell Assembly Patterns during Sharp Wave-Ripples , 2016, Neuron.

[297]  D. Olton,et al.  Cholinergic manipulations in the medial septal area: age-related effects on working memory and hippocampal electrophysiology , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[298]  A. Björklund,et al.  Spatial learning impairments in rats with selective immunolesion of the forebrain cholinergic system. , 1992, Neuroreport.

[299]  John A. King,et al.  How vision and movement combine in the hippocampal place code , 2012, Proceedings of the National Academy of Sciences.

[300]  I. Gritti,et al.  Parvalbumin, calbindin, or calretinin in cortically projecting and GABAergic, cholinergic, or glutamatergic basal forebrain neurons of the rat , 2003, The Journal of comparative neurology.

[301]  Arne D. Ekstrom,et al.  Cellular networks underlying human spatial navigation , 2003, Nature.

[302]  T. Robbins,et al.  The role of cortical cholinergic afferent projections in cognition: impact of new selective immunotoxins , 2000, Behavioural Brain Research.

[303]  N. Burgess,et al.  The Cognitive Architecture of Spatial Navigation: Hippocampal and Striatal Contributions , 2015, Neuron.

[304]  J. Coyle,et al.  Alzheimer's disease and senile dementia: loss of neurons in the basal forebrain. , 1982, Science.

[305]  Laszlo Zaborszky,et al.  The Input-Output Relationship of the Cholinergic Basal Forebrain. , 2017, Cell reports.

[306]  D. Hassabis,et al.  A Goal Direction Signal in the Human Entorhinal/Subicular Region , 2015, Current Biology.

[307]  S. Heckers,et al.  Differential effects on spatial navigation of immunotoxin-induced cholinergic lesions of the medial septal area and nucleus basalis magnocellularis , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[308]  Nancy J. Woolf,et al.  Cholinergic systems in mammalian brain and spinal cord , 1991, Progress in Neurobiology.

[309]  Michael E. Hasselmo,et al.  Neuromodulation, theta rhythm and rat spatial navigation , 2002, Neural Networks.

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

[311]  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.

[312]  F. Bermúdez-Rattoni,et al.  Activation of hippocampal postsynaptic muscarinic receptors is involved in long‐term spatial memory formation , 2007, The European journal of neuroscience.

[313]  J. Donders,et al.  GRAND ROUNDS: Topographical Heading Disorientation - A Case Study , 2006 .

[314]  Kathryn A Davis,et al.  Electrophysiological Signatures of Spatial Boundaries in the Human Subiculum , 2017, The Journal of Neuroscience.

[315]  Masahiko Watanabe,et al.  Medial septal GABAergic projection neurons promote object exploration behavior and type 2 theta rhythm , 2016, Proceedings of the National Academy of Sciences.

[316]  B. Kutty,et al.  Cholinergic immunotoxin 192 IgG-SAPORIN alters subicular theta–gamma activity and impairs spatial learning in rats , 2014, Neurobiology of Learning and Memory.

[317]  T. Arendt,et al.  Alzheimer plaques and cortical cholinergic innervation , 1986, Neuroscience.

[318]  G. Rainer,et al.  Basal forebrain contributes to default mode network regulation , 2018, Proceedings of the National Academy of Sciences.

[319]  T. Kameyama,et al.  Cholinergic receptor agonists inhibit pirenzepine-induced dysfunction of spontaneous alternation performance in the mouse. , 1995, General pharmacology.

[320]  Yukio Ichitani,et al.  Nicotine improves AF64A-induced spatial memory deficits in Morris water maze in rats , 2010, Neuroscience Letters.

[321]  Bingni W. Brunton,et al.  Rats and Humans Can Optimally Accumulate Evidence for Decision-Making , 2013, Science.

[322]  Martin Fuhrmann,et al.  Locomotion, Theta Oscillations, and the Speed-Correlated Firing of Hippocampal Neurons Are Controlled by a Medial Septal Glutamatergic Circuit , 2015, Neuron.

[323]  T. Robbins,et al.  Central cholinergic systems and cognition. , 1997, Annual review of psychology.

[324]  Vaughn L. Hetrick,et al.  Cortical cholinergic signaling controls the detection of cues , 2016, Proceedings of the National Academy of Sciences.

[325]  A. Chiba,et al.  Task-phase-specific dynamics of basal forebrain neuronal ensembles , 2014, Front. Syst. Neurosci..

[326]  H. Kondo,et al.  Topographic organization of the basal forebrain projections to the perirhinal, postrhinal, and entorhinal cortex in rats , 2016, The Journal of comparative neurology.

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

[328]  G. Riva,et al.  From allo- to egocentric spatial ability in early Alzheimer’s disease: A study with virtual reality spatial tasks , 2013, Cognitive neuroscience.

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

[330]  P. E. Gold,et al.  Impaired and spared cholinergic functions in the hippocampus after lesions of the medial septum/vertical limb of the diagonal band with 192 IgG‐saporin , 2004, Hippocampus.

[331]  Mayank R. Mehta,et al.  Multisensory Control of Hippocampal Spatiotemporal Selectivity , 2013, Science.

[332]  J. Yakel,et al.  Cholinergic modulation of the hippocampal region and memory function , 2017, Journal of neurochemistry.

[333]  L. Bianchi,et al.  Effects of novelty and habituation on acetylcholine, GABA, and glutamate release from the frontal cortex and hippocampus of freely moving rats , 2001, Neuroscience.

[334]  Jill K. Leutgeb,et al.  Grid and Nongrid Cells in Medial Entorhinal Cortex Represent Spatial Location and Environmental Features with Complementary Coding Schemes , 2017, Neuron.

[335]  K. Baskerville,et al.  Topography of cholinergic afferents from the nucleus basalis of meynert to representational areas of sensorimotor cortices in the rat , 1993, The Journal of comparative neurology.

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

[337]  G. Buzsáki,et al.  Nucleus basalis and thalamic control of neocortical activity in the freely moving rat , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[338]  Pierre-Pascal Lenck-Santini,et al.  Speed modulation of hippocampal theta frequency correlates with spatial memory performance , 2013, Hippocampus.

[339]  J. Klein,et al.  Microdialysis and its use in behavioural studies: Focus on acetylcholine , 2017, Journal of Neuroscience Methods.

[340]  A. Disney,et al.  Is There a Canonical Cortical Circuit for the Cholinergic System? Anatomical Differences Across Common Model Systems , 2018, Front. Neural Circuits.

[341]  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.

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

[343]  L. Rondi-Reig,et al.  The cerebellum: a new key structure in the navigation system , 2013, Front. Neural Circuits.

[344]  Trevor W Robbins,et al.  Cholinergic modulation of visual attention and working memory: dissociable effects of basal forebrain 192-IgG-saporin lesions and intraprefrontal infusions of scopolamine. , 2004, Learning & memory.

[345]  Dharshan Kumaran,et al.  The Human Hippocampus: Cognitive Maps or Relational Memory? , 2005, The Journal of Neuroscience.

[346]  Malin Björnsdotter,et al.  Posterior Cingulate Cortex Integrates the Senses of Self-Location and Body Ownership , 2015, Current Biology.

[347]  B. McNaughton,et al.  Spatial representation in the hippocampal formation: a history , 2017, Nature Neuroscience.

[348]  Corbett Bennett,et al.  Prolonged Disynaptic Inhibition in the Cortex Mediated by Slow, Non-α7 Nicotinic Excitation of a Specific Subset of Cortical Interneurons , 2012, The Journal of Neuroscience.

[349]  J. Taube,et al.  Behavioral/systems/cognitive Hippocampal Place Cell Instability after Lesions of the Head Direction Cell Network , 2022 .

[350]  R. Bartus,et al.  The cholinergic hypothesis of geriatric memory dysfunction. , 1982, Science.

[351]  P. Sanberg,et al.  Nicotine enhances morris water maze performance of young and aged rats , 1995, Neurobiology of Aging.

[352]  David A. Johnson,et al.  Selective lesion of cholinergic neurons in the medial septum by 192 IgG-saporin impairs learning in a delayed matching to position T-maze paradigm , 2002, Brain Research.

[353]  M. Tsanov Speed and Oscillations: Medial Septum Integration of Attention and Navigation , 2017, Front. Syst. Neurosci..

[354]  R. Poldrack,et al.  Competition among multiple memory systems: converging evidence from animal and human brain studies , 2003, Neuropsychologia.

[355]  Susana Q. Lima,et al.  PINP: A New Method of Tagging Neuronal Populations for Identification during In Vivo Electrophysiological Recording , 2009, PloS one.

[356]  M. Frotscher,et al.  Organization of the septal region in the rat brain: Cholinergic‐GABAergic interconnections and the termination of hippocampo‐septal fibers , 1989, The Journal of comparative neurology.

[357]  C. Pittenger,et al.  A double dissociation revealing bidirectional competition between striatum and hippocampus during learning , 2008, Proceedings of the National Academy of Sciences.

[358]  Alison L. Barth,et al.  Precisely Timed Nicotinic Activation Drives SST Inhibition in Neocortical Circuits , 2018, Neuron.

[359]  B. Bontempi,et al.  SIB-1553A, (+/-)-4-[[2-(1-methyl-2-pyrrolidinyl)ethyl]thio]phenol hydrochloride, a subtype-selective ligand for nicotinic acetylcholine receptors with putative cognitive-enhancing properties: effects on working and reference memory performances in aged rodents and nonhuman primates. , 2001, The Journal of pharmacology and experimental therapeutics.

[360]  Katherine R. Sherrill,et al.  Hippocampus and Retrosplenial Cortex Combine Path Integration Signals for Successful Navigation , 2013, The Journal of Neuroscience.

[361]  L. Savage,et al.  Selective septohippocampal – but not forebrain amygdalar – cholinergic dysfunction in diencephalic amnesia , 2007, Brain Research.

[362]  M. Decker,et al.  Differential effects of medial septal lesions on spatial-memory tasks , 1992, Psychobiology.

[363]  M. Lochner,et al.  The muscarinic antagonists scopolamine and atropine are competitive antagonists at 5-HT3 receptors , 2016, Neuropharmacology.

[364]  M. Gallagher,et al.  Intact spatial learning following lesions of basal forebrain cholinergic neurons. , 1996, Neuroreport.

[365]  J. O’Neill,et al.  Reactivation of experience-dependent cell assembly patterns in the hippocampus , 2008, Nature Neuroscience.

[366]  M. Decker,et al.  Effects of systemic and intracerebroventricular administration of mecamylamine, a nicotinic cholinergic antagonist, on spatial memory in rats , 2005, Psychopharmacology.

[367]  Aiden E. G. F. Arnold,et al.  A critical review of the allocentric spatial representation and its neural underpinnings: toward a network-based perspective , 2014, Front. Hum. Neurosci..

[368]  Larry L. Butcher,et al.  Cholinergic projections from the basal forebrain to frontal, parietal, temporal, occipital, and cingulate cortices: A combined fluorescent tracer and acetylcholinesterase analysis , 1982, Brain Research Bulletin.

[369]  A. V Olypher,et al.  Quantifying location-specific information in the discharge of rat hippocampal place cells , 2003, Journal of Neuroscience Methods.

[370]  Benjamin J Clark,et al.  The Retrosplenial-Parietal Network and Reference Frame Coordination for Spatial Navigation , 2018, Behavioral neuroscience.

[371]  Michael Hasselmo,et al.  Modulation of Hippocampal Circuits by Muscarinic and Nicotinic Receptors , 2017, Front. Neural Circuits.

[372]  Guy B. Williams,et al.  The relationship of topographical memory performance to regional neurodegeneration in Alzheimer's disease , 2012, Front. Ag. Neurosci..

[373]  J. Aggleton,et al.  A comparison of egocentric and allocentric spatial memory in a patient with selective hippocampal damage , 2000, Neuropsychologia.

[374]  J. Kehr,et al.  Intraseptal muscarinic ligands and galanin: influence on hippocampal acetylcholine and cognition , 2004, Neuroscience.

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

[376]  John P. Aggleton,et al.  Effects of selective granular retrosplenial cortex lesions on spatial working memory in rats , 2010, Behavioural Brain Research.

[377]  E. Maguire,et al.  The Well-Worn Route and the Path Less Traveled Distinct Neural Bases of Route Following and Wayfinding in Humans , 2003, Neuron.

[378]  D. Bertrand,et al.  Nicotinic acetylcholine receptors and nicotinic cholinergic mechanisms of the central nervous system. , 2007, Annual review of pharmacology and toxicology.

[379]  D. Olton,et al.  Cholinergic and GABAergic modulation of medial septal area: effect on working memory. , 1990, Behavioral neuroscience.

[380]  L. Colom,et al.  Characterization of medial septal glutamatergic neurons and their projection to the hippocampus , 2005, Synapse.

[381]  R. Gaykema,et al.  Cortical input to the basal forebrain , 1997, Neuroscience.

[382]  Elizabeth R. Chrastil,et al.  Functional connections between optic flow areas and navigationally responsive brain regions during goal-directed navigation , 2015, NeuroImage.

[383]  M. Giovannini,et al.  Cholinesterase inhibitors and memory. , 2010, Chemico-biological interactions.

[384]  G. Lubec,et al.  Scopolamine Administration Modulates Muscarinic, Nicotinic and NMDA Receptor Systems , 2012, PloS one.

[385]  E D Levin,et al.  Effects of the nicotinic receptor blocker mecamylamine on radial-arm maze performance in rats. , 1987, Behavioral and neural biology.

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

[387]  Tamás F. Freund,et al.  GABAergic septohippocampal neurons contain parvalbumin , 1989, Brain Research.

[388]  N. Fortin,et al.  Nonspatial Sequence Coding in CA1 Neurons , 2016, The Journal of Neuroscience.

[389]  P. E. Gold,et al.  Switching Memory Systems during Learning: Changes in Patterns of Brain Acetylcholine Release in the Hippocampus and Striatum in Rats , 2003, The Journal of Neuroscience.

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

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

[392]  E. Levin,et al.  Ventral hippocampal ibotenic acid lesions block chronic nicotine-induced spatial working memory improvement in rats. , 1999, Brain research. Cognitive brain research.

[393]  Laura Lee Colgin,et al.  Impairments in spatial representations and rhythmic coordination of place cells in the 3xTg mouse model of Alzheimer's disease , 2017, Hippocampus.

[394]  N. Takahashi,et al.  Pure topographic disorientation due to right retrosplenial lesion , 1997, Neurology.

[395]  Roddy M. Grieves,et al.  Lesions of the Head Direction Cell System Increase Hippocampal Place Field Repetition , 2017, Current Biology.

[396]  James G. Heys,et al.  Possible role of acetylcholine in regulating spatial novelty effects on theta rhythm and grid cells , 2012, Front. Neural Circuits.

[397]  L. Hersh,et al.  An atlas of the regional and laminar distribution of choline acetyltransferase immunoreactivity in rat cerebral cortex , 1989, Neuroscience.

[398]  L. Squire,et al.  The medial temporal lobe memory system , 1991, Science.

[399]  C. Lazarus,et al.  Combined lesions of cholinergic and serotonergic neurons in the rat brain using 192 IgG‐saporin and 5,7‐dihydroxytryptamine: neurochemical and behavioural characterization , 2000, The European journal of neuroscience.

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

[401]  C. D. de Kock,et al.  Layer-specific cholinergic control of human and mouse cortical synaptic plasticity , 2016, Nature Communications.

[402]  Wei-Cheng Chang,et al.  Cell type-specific long-range connections of basal forebrain circuit , 2016, eLife.

[403]  Charles J Duffy,et al.  Detecting navigational deficits in cognitive aging and Alzheimer disease using virtual reality , 2008, Neurology.

[404]  T. Freund,et al.  Cholinergic synapses in the rat brain: a correlated light and electron microscopic immunohistochemical study employing a monoclonal antibody against choline acetyltransferase , 1984, Brain Research.

[405]  S. El Mestikawy,et al.  Vesicular glutamate transporter 3 immunoreactivity is present in cholinergic basal forebrain neurons projecting to the basolateral amygdala in rat , 2006, The Journal of comparative neurology.

[406]  T. J. Walsh,et al.  Behavioral and neurobiological alterations induced by the immunotoxin 192-IgG-saporin: cholinergic and non-cholinergic effects following i.c.v. injection , 1995, Brain Research.

[407]  Tamás Kiss,et al.  How do glutamatergic and GABAergic cells contribute to synchronization in the medial septum? , 2006, Journal of Computational Neuroscience.

[408]  B. Platt,et al.  The cholinergic system and spatial learning , 2011, Behavioural Brain Research.

[409]  Stephan Heckers,et al.  Hippocampus at 25 , 2016, Hippocampus.

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

[411]  Optogenetic excitation of cholinergic inputs to hippocampus primes future contextual fear associations , 2017, Scientific Reports.

[412]  D. Price,et al.  Identification and localization of muscarinic acetylcholine receptor proteins in brain with subtype-specific antibodies , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[413]  C. Lustig,et al.  Deterministic functions of cortical acetylcholine , 2014, The European journal of neuroscience.

[414]  J. Phillis,et al.  Acetylcholine release from the central nervous system: a 50-year retrospective. , 2005, Critical reviews in neurobiology.

[415]  Douglas A Nitz,et al.  Spaces within spaces: rat parietal cortex neurons register position across three reference frames , 2012, Nature Neuroscience.

[416]  Johannes J. Letzkus,et al.  A disinhibitory microcircuit for associative fear learning in the auditory cortex , 2011, Nature.

[417]  J. Price,et al.  Individual cells in the nucleus basalis-diagonal band complex have restricted axonal projections to the cerebral cortex in the rat , 1983, Brain Research.

[418]  S. Mizumori,et al.  Basal ganglia contributions to adaptive navigation , 2009, Behavioural Brain Research.

[419]  Janina Ferbinteanu,et al.  Contributions of Hippocampus and Striatum to Memory-Guided Behavior Depend on Past Experience , 2016, The Journal of Neuroscience.

[420]  M. Danik,et al.  Distinct electrophysiological properties of glutamatergic, cholinergic and GABAergic rat septohippocampal neurons: novel implications for hippocampal rhythmicity , 2003, The Journal of physiology.

[421]  R. Lukas,et al.  A Novel Nicotinic Acetylcholine Receptor Subtype in Basal Forebrain Cholinergic Neurons with High Sensitivity to Amyloid Peptides , 2009, The Journal of Neuroscience.

[422]  Michael E. Hasselmo,et al.  A Proposed Function for Hippocampal Theta Rhythm: Separate Phases of Encoding and Retrieval Enhance Reversal of Prior Learning , 2002, Neural Computation.

[423]  S. Dudek,et al.  Hippocampus and Entorhinal Cortex Recruit Cholinergic and NMDA Receptors Separately to Generate Hippocampal Theta Oscillations. , 2017, Cell reports.

[424]  T. Maviel,et al.  Role of central cholinergic receptor sub-types in spatial working memory: a five-arm maze task in mice provides evidence for a functional role of nicotinic receptors in mediating trace access processes , 2003, Neuroscience.

[425]  O. Pedraza,et al.  Daytime sleepiness in dementia with Lewy bodies is associated with neuronal depletion of the nucleus basalis of Meynert. , 2018, Parkinsonism & related disorders.

[426]  F. Mormann,et al.  Synergy of Direct and Indirect Cholinergic Septo-Hippocampal Pathways Coordinates Firing in Hippocampal Networks , 2015, The Journal of Neuroscience.

[427]  F. Motamedi,et al.  Effects of reversible inactivations of the medial septal area on reference and working memory versions of the Morris water maze , 1996, Brain Research.

[428]  D. Harper,et al.  Differential effects of MDMA and scopolamine on working versus reference memory in the radial arm maze task , 2010, Neurobiology of Learning and Memory.

[429]  Seralynne D Vann,et al.  Extensive cytotoxic lesions of the rat retrosplenial cortex reveal consistent deficits on tasks that tax allocentric spatial memory. , 2002, Behavioral neuroscience.

[430]  T. J. Walsh,et al.  Injection of IgG 192-saporin into the medial septum produces cholinergic hypofunction and dose-dependent working memory deficits , 1996, Brain Research.

[431]  Z. Nadasdy,et al.  The Basal Forebrain Corticopetal System Revisited , 1999, Annals of the New York Academy of Sciences.

[432]  Ales Stuchlik,et al.  Drugs Interfering with Muscarinic Acetylcholine Receptors and Their Effects on Place Navigation , 2017, Front. Psychiatry.

[433]  R. Kesner,et al.  Medial septal and nucleus basalis magnocellularis lesions produce order memory deficits in rats which mimic symptomatology of Alzheimer's disease , 1986, Neurobiology of Aging.

[434]  David Dupret,et al.  Behavior-Dependent Activity and Synaptic Organization of Septo-hippocampal GABAergic Neurons Selectively Targeting the Hippocampal CA3 Area , 2017, Neuron.

[435]  R. Sutherland,et al.  Contributions of cingulate cortex to two forms of spatial learning and memory , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[437]  Martin Sarter,et al.  Acetylcholine Release in Prefrontal Cortex Promotes Gamma Oscillations and Theta–Gamma Coupling during Cue Detection , 2017, The Journal of Neuroscience.

[438]  A. Losonczy,et al.  Regulation of neuronal input transformations by tunable dendritic inhibition , 2012, Nature Neuroscience.

[439]  V. Alvarez,et al.  Distinctive Modulation of Dopamine Release in the Nucleus Accumbens Shell Mediated by Dopamine and Acetylcholine Receptors , 2017, The Journal of Neuroscience.

[440]  E Valenstein,et al.  Retrosplenial amnesia. , 1987, Brain : a journal of neurology.

[441]  William Wisden,et al.  Dual-transmitter systems regulating arousal, attention, learning and memory , 2018, Neuroscience & Biobehavioral Reviews.

[442]  D. Menétrey,et al.  Cholinergic and peptidergic projections from the medial septum and the nucleus of the diagonal band of broca to dorsal hippocampus, cingulate cortex and olfactory bulb: A combined wheatgerm agglutinin-apohorseradish peroxidase-gold immunohistochemical study , 1989, Neuroscience.

[443]  C. Geula,et al.  Complete and selective cholinergic denervation of rat neocortex and hippocampus but not amygdala by an immunotoxin against the p75 NGF receptor , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[444]  Douglas A Nitz,et al.  Retrosplenial cortex maps the conjunction of internal and external spaces , 2015, Nature Neuroscience.

[445]  K. Amunts,et al.  Reduction of basal forebrain cholinergic system parallels cognitive impairment in patients at high risk of developing Alzheimer's disease. , 2010, Cerebral cortex.

[446]  J. E. Vaughn,et al.  An immunocytochemical study of choline acetyltransferase- containing neurons and axon terminals in normal and partially deafferented hippocampal formation , 1987, Brain Research.

[447]  E. Levin,et al.  Nicotinic antagonist administration into the ventral hippocampus and spatial working memory in rats , 1997, Neuroscience.

[448]  A. Nagaoka,et al.  Characteristics of memory impairment following lesioning of the basal forebrain and medial septal nucleus in rats , 1987, Brain Research.

[449]  Z. Borhegyi,et al.  GABAergic Neurons of the Medial Septum Lead the Hippocampal Network during Theta Activity , 2009, The Journal of Neuroscience.

[450]  Ágoston Török,et al.  Context-dependent spatially periodic activity in the human entorhinal cortex , 2017, Proceedings of the National Academy of Sciences.

[451]  Jan Laczó,et al.  Behavioral Neuroscience Mini Review Article Neural Correlates of Spatial Navigation Changes in Mild Cognitive Impairment and Alzheimer's Disease , 2022 .

[452]  Yang Dan,et al.  Cell-type-specific modulation of neocortical activity by basal forebrain input , 2013, Front. Syst. Neurosci..

[453]  F. Eckenstein,et al.  An anatomical study of cholinergic innervation in rat cerebral cortex , 1988, Neuroscience.

[454]  D. Ji,et al.  Hippocampal awake replay in fear memory retrieval , 2017, Nature Neuroscience.

[455]  Bruno Poucet,et al.  Functional interaction between the associative parietal cortex and hippocampal place cell firing in the rat , 2005, The European journal of neuroscience.

[456]  K. Frick,et al.  Oxotremorine infusions into the medial septal area of middle-aged rats affect spatial reference memory and ChAT activity , 1996, Behavioural Brain Research.

[457]  Eleanor A Maguire,et al.  Retrosplenial Cortex Indexes Stability beyond the Spatial Domain , 2018, The Journal of Neuroscience.

[458]  A. Fagan,et al.  Spatial Navigation in Preclinical Alzheimer's Disease. , 2016, Journal of Alzheimer's disease : JAD.

[459]  Georg B. Keller,et al.  A Sensorimotor Circuit in Mouse Cortex for Visual Flow Predictions , 2017, Neuron.

[460]  Denis Pare,et al.  Impact of Basal Forebrain Cholinergic Inputs on Basolateral Amygdala Neurons , 2015, The Journal of Neuroscience.