Changes in hippocampal excitatory synaptic transmission during cholinergically induced theta and slow oscillation states

Neural processing in the hippocampus (HPC) during sleep is important for declarative memory storage. Previously, we have shown that alternations of sleep‐like REM and non‐REM brain states that involve changing patterns of synchronized oscillatory network activity in the HPC [i.e., theta and the slow oscillation (SO), respectively] robustly and differentially influence excitatory synaptic transmission in a variety of hippocampal pathways. Given that state in the HPC is dependent on variations in cholinergic tone in both sleep and under urethane anesthesia, in the present study we induced theta and SO states via systemic cholinergic manipulations in urethane‐anesthetized rats to confirm similar changes in synaptic responsiveness. This was conducted using linear multiprobe recordings and current source density analysis of electrically evoked potentials in commissural and temporal ammonic inputs to CA1 and medial and lateral perforant path inputs to dentate gyrus (DG). Cholinergic agonism and antagonism induced theta and the SO, respectively, and similarly to the case with spontaneous states, also diminished and promoted, respectively, excitatory synaptic currents in all pathways (except for the medial perforant path input to DG which showed the opposite modulation). These results suggest that both state and cholinergic tone bias the hippocampal network during natural sleep across REM and non‐REM episodes and that this modulation may play an important role in the consolidation of declarative memories. © 2009 Wiley‐Liss, Inc.

[1]  J. Born,et al.  Odor Cues During Slow-Wave Sleep Prompt Declarative Memory Consolidation , 2007, Science.

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

[3]  H. Eichenbaum.  Hippocampus Cognitive Processes and Neural Representations that Underlie Declarative Memory , 2004, Neuron.

[4]  C. Bramham,et al.  Synaptic plasticity in the hippocampus is modulated by behavioral state , 1989, Brain Research.

[5]  J. Winson,et al.  Gating of neuronal transmission in the hippocampus: efficacy of transmission varies with behavioral state. , 1977, Science.

[6]  O. Steward,et al.  Cells of origin of entorhinal cortical afferents to the hippocampus and fascia dentata of the rat , 1976, The Journal of comparative neurology.

[7]  Elizabeth A. Clement,et al.  Cyclic and Sleep-Like Spontaneous Alternations of Brain State Under Urethane Anaesthesia , 2008, PloS one.

[8]  J. Lerma,et al.  Sensory modulation of hippocampal transmission. II. Evidence for a cholinergic locus of inhibition in the Schaffer-CA1 synapse , 1988, Brain Research.

[9]  G. Lynch,et al.  Septal modulation of excitatory transmission in hippocampus. , 2003, Journal of neurophysiology.

[10]  L. Stan Leung,et al.  Behavior-dependent evoked potentials in the hippocampal CA1 region of the rat. I. Correlation with behavior and egg , 1980, Brain Research.

[11]  L. Haberly,et al.  Analysis of synaptic events in the opossum piriform cortex with improved current source-density techniques. , 1989, Journal of neurophysiology.

[12]  G Buzsáki,et al.  Memory consolidation during sleep: a neurophysiological perspective. , 1998, Journal of sleep research.

[13]  F. Kloosterman,et al.  Physiology of the Entorhinal and Perirhinal Projections to the Hippocampus Studied by Current Source Density Analysis , 2000, Annals of the New York Academy of Sciences.

[14]  A. Alonso,et al.  Differential electroresponsiveness of stellate and pyramidal-like cells of medial entorhinal cortex layer II. , 1993, Journal of neurophysiology.

[15]  J. Sarvey,et al.  Norepinephrine induces pathway-specific long-lasting potentiation and depression in the hippocampal dentate gyrus. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[16]  M Segal.  A correlation between hippocampal responses to interhemispheric stimulation, hippocampal slow rhythmic activity and behaviour. , 1978, Electroencephalography and clinical neurophysiology.

[17]  Jørn Hounsgaard,et al.  Presynaptic inhibitory action of acetylcholine in area CA1 of the hippocampus , 1978, Experimental Neurology.

[18]  J. Born,et al.  Declarative memory consolidation: mechanisms acting during human sleep. , 2004, Learning & memory.

[19]  J. Winson,et al.  Neuronal transmission through hippocampal pathways dependent on behavior. , 1978, Journal of neurophysiology.

[20]  R. Dingledine,et al.  Presynaptic inhibitory effect of acetylcholine in the hippocampus , 1981, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

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

[23]  R. J. McDonald,et al.  Lesions of the medial or lateral perforant path have different effects on hippocampal contributions to place learning and on fear conditioning to context , 1999, Behavioural Brain Research.

[24]  Y. Ben-Ari,et al.  Opposite actions of muscarinic and nicotinic agents on hippocampal dendritic negative fields recorded in rats , 1982, Neuropharmacology.

[25]  M. Witter,et al.  Anatomical Organization of the Parahippocampal‐Hippocampal Network , 2000, Annals of the New York Academy of Sciences.

[26]  M. Moser,et al.  Impaired Spatial Representation in CA1 after Lesion of Direct Input from Entorhinal Cortex , 2008, Neuron.

[27]  C. Pavlides,et al.  Long-term potentiation in the dentate gyrus is induced preferentially on the positive phase of θ-rhythm , 1988, Brain Research.

[28]  B Milner,et al.  Loss of recent memory after bilateral hippocampal lesions. 1957. , 1996, The Journal of neuropsychiatry and clinical neurosciences.

[29]  Lorand Kellenyi,et al.  Changes in neuronal transmission in the rat hippocampus during behavior , 1981, Brain Research.

[30]  F. H. Lopes da Silva,et al.  Two reentrant pathways in the hippocampal‐entorhinal system , 2004, Hippocampus.

[31]  R. Anwyl,et al.  Stimulation on the Positive Phase of Hippocampal Theta Rhythm Induces Long-Term Potentiation That Can Be Depotentiated by Stimulation on the Negative Phase in Area CA1 In Vivo , 1997, The Journal of Neuroscience.

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

[33]  J. Lisman,et al.  Bidirectional synaptic plasticity induced by a single burst during cholinergic theta oscillation in CA1 in vitro , 1995, Neuron.

[34]  M. Hasselmo,et al.  Size of CA1-evoked synaptic potentials is related to theta rhythm phase in rat hippocampus. , 2000, Journal of neurophysiology.

[35]  D. Amaral,et al.  The Hippocampal Formation , 2009 .

[36]  Lisa M. Giocomo,et al.  Temporal Frequency of Subthreshold Oscillations Scales with Entorhinal Grid Cell Field Spacing , 2007, Science.

[37]  C. Pavlides,et al.  Long-term potentiation in the dentate gyrus is induced preferentially on the positive phase of theta-rhythm. , 1988, Brain research.

[38]  Elizabeth A. Clement,et al.  Hippocampal Slow Oscillation: A Novel EEG State and Its Coordination with Ongoing Neocortical Activity , 2006, The Journal of Neuroscience.

[39]  Wickliffe C. Abraham,et al.  Differences in synaptic transmission between medial and lateral components of the perforant path , 1984, Brain Research.

[40]  B. Tahvildari,et al.  Morphological and electrophysiological properties of lateral entorhinal cortex layers II and III principal neurons , 2005, The Journal of comparative neurology.

[41]  K. J. Canning,et al.  Entorhinal inputs to hippocampal CA1 and dentate gyrus in the rat: a current-source-density study. , 1995, Journal of neurophysiology.

[42]  J. Knierim,et al.  Hippocampal place cells: Parallel input streams, subregional processing, and implications for episodic memory , 2006, Hippocampus.

[43]  J. Lisman,et al.  Low-frequency stimulation at the troughs of theta-oscillation induces long-term depression of previously potentiated CA1 synapses. , 1996, Journal of neurophysiology.

[44]  Björn Rasch,et al.  Combined Blockade of Cholinergic Receptors Shifts the Brain from Stimulus Encoding to Memory Consolidation , 2006, Journal of Cognitive Neuroscience.

[45]  J. Lerma,et al.  Sensory modulation of hippocampal transmission. I. Opposite effects on CA1 and dentate gyrus synapsis , 1988, Brain Research.

[46]  B. L. McNaughton,et al.  Evidence for two physiologically distinct perforant pathways to the fascia dentata , 1980, Brain Research.

[47]  L. Squire.  Memory and the hippocampus: a synthesis from findings with rats, monkeys, and humans. , 1992, Psychological review.

[48]  M. Witter.  Organization of the entorhinal—hippocampal system: A review of current anatomical data , 1993, Hippocampus.

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

[50]  C. Nicholson,et al.  Theory of current source-density analysis and determination of conductivity tensor for anuran cerebellum. , 1975, Journal of neurophysiology.

[51]  B. H. Bland.  The physiology and pharmacology of hippocampal formation theta rhythms , 1986, Progress in Neurobiology.

[52]  L. Leung,et al.  Spectral analysis of hippocampal EEG in the freely moving rat: effects of centrally active drugs and relations to evoked potentials. , 1985, Electroencephalography and clinical neurophysiology.

[53]  M. Hasselmo.  Neuromodulation: acetylcholine and memory consolidation , 1999, Trends in Cognitive Sciences.

[54]  J. Knierim,et al.  Major Dissociation Between Medial and Lateral Entorhinal Input to Dorsal Hippocampus , 2005, Science.

[55]  O. Steward,et al.  Topographic organization of the projections from the entorhinal area to the hippocampal formation of the rat , 1976, The Journal of comparative neurology.

[56]  C. Dickson,et al.  Rhythmic constraints on hippocampal processing: state and phase-related fluctuations of synaptic excitability during theta and the slow oscillation. , 2008, Journal of neurophysiology.

[57]  K L Ketchum,et al.  Synaptic events that generate fast oscillations in piriform cortex , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[58]  C. Cotman,et al.  Carbachol depresses synaptic responses in the medial but not the lateral perforant path , 1989, Brain Research.

[59]  Avery Tung,et al.  Anesthesia and sleep. , 2004, Sleep medicine reviews.

[60]  J. Sarvey,et al.  NMDA receptor antagonists reduce medial, but not lateral, perforant path-evoked EPSPs in dentate gyrus of rat hippocampal slice , 2004, Experimental Brain Research.

[61]  Y. Ben-Ari,et al.  Dual cholinergic modulation of hippocampal somatic and dendritic field potentials by the septo-hippocampal pathway , 2004, Experimental Brain Research.

[62]  E. Schuman,et al.  Role for a cortical input to hippocampal area CA1 in the consolidation of a long-term memory , 2004, Nature.

[63]  Kara L. Agster,et al.  Functional neuroanatomy of the parahippocampal region: The lateral and medial entorhinal areas , 2007, Hippocampus.

[64]  C. H. Vanderwolf,et al.  Behavior-dependent evoked potentials in the hippocampal CA1 region of the rat. II. Effect of eserine, atropine, ether and pentobarbital , 1980, Brain Research.

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

[66]  Howard Eichenbaum,et al.  Remembering: Functional Organization of the Declarative Memory System , 2006, Current Biology.

[67]  J. Born,et al.  Sleep to Remember , 2006, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[68]  C. Davies,et al.  Cholinergic modulation of hippocampal cells and circuits , 2005, The Journal of physiology.

[69]  C. H. Vanderwolf.  Cerebral activity and behavior: control by central cholinergic and serotonergic systems. , 1988, International review of neurobiology.

[70]  G. Buzsáki.  Theta Oscillations in the Hippocampus , 2002, Neuron.

[71]  M. Hasselmo,et al.  Laminar selectivity of the cholinergic suppression of synaptic transmission in rat hippocampal region CA1: computational modeling and brain slice physiology , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[72]  C. Nicholson,et al.  Experimental optimization of current source-density technique for anuran cerebellum. , 1975, Journal of neurophysiology.

[73]  M. Hasselmo,et al.  Stimulation in Hippocampal Region CA1 in Behaving Rats Yields Long-Term Potentiation when Delivered to the Peak of Theta and Long-Term Depression when Delivered to the Trough , 2003, The Journal of Neuroscience.