Book contents
- Frontmatter
- Contents
- List of contributors
- Part I Introduction
- Part II Organization of neuronal activity in neuronal populations
- Part III Neuronal population information coding and plasticity in specific brain areas
- 7 Functional roles of theta and gamma oscillations in the association and dissociation of neuronal networks in primates and rodents
- 8 Theta rhythm and bidirectional plasticity in the hippocampus
- 9 Distributed population codes in sensory and memory representations of the neocortex
- 10 The role of neuronal populations in auditory cortex for category learning
- 11 The construction of olfactory representations
- Part IV Functional integration of different brain areas in information processing and plasticity
- Part V Disturbances of population activity as the basis of schizophrenia
- Part VI Summary, conclusion, and future targets
- Index
- References
8 - Theta rhythm and bidirectional plasticity in the hippocampus
Published online by Cambridge University Press: 14 August 2009
Book contents
- Frontmatter
- Contents
- List of contributors
- Part I Introduction
- Part II Organization of neuronal activity in neuronal populations
- Part III Neuronal population information coding and plasticity in specific brain areas
- 7 Functional roles of theta and gamma oscillations in the association and dissociation of neuronal networks in primates and rodents
- 8 Theta rhythm and bidirectional plasticity in the hippocampus
- 9 Distributed population codes in sensory and memory representations of the neocortex
- 10 The role of neuronal populations in auditory cortex for category learning
- 11 The construction of olfactory representations
- Part IV Functional integration of different brain areas in information processing and plasticity
- Part V Disturbances of population activity as the basis of schizophrenia
- Part VI Summary, conclusion, and future targets
- Index
- References
Summary
Introduction
The local field potential from the hippocampus of an awake, stationary animal is filled with seemingly random low-amplitude high-frequency activity and arrhythmic high-amplitude low-frequency activity. To the untrained eye it is nearly impossible to discern any clear patterns or relationships of the signal to behavior, as the local field potential appears to be only noise. Then something striking happens, as the animal starts to move around, an extremely rhythmic high-amplitude 6–10-Hz sinusoidal waveform appears and instantly offers a window into the relationship between the hippocampal field potential and the animal's behavior. When Green and Arduini (1954) first recorded local field potentials activity from the hippocampus of behaving animals they saw this rhythmic activity (theta rhythm; 6–10-Hz high-amplitude sinusoidal activity: Buzsáki et al., 1986) and it was clear to them that theta rhythm played a significant role in hippocampal function. Theta appeared whenever the animal walked, ran, sniffed, oriented, reared, or went into rapid eye movement (REM) sleep, and theta was notably absent during consummatory behaviors (eating and drinking), grooming, and slow wave sleep.
The nature of theta's role in hippocampal processing was somewhat clarified when studies of the effect of hippocampectomy in humans and rodents were performed, and the hippocampus's central role in associative memory was suggested (Scoville and Milner, 1957; Morris et al., 1982). Since those original studies, further work has shown memory impairments in a wide range of behavioral and cognitive tasks that utilize multiple sensory modalities and behavioral responses (Eichenbaum, 2000).
- Type
- Chapter
- Information
- Information Processing by Neuronal Populations , pp. 174 - 191Publisher: Cambridge University PressPrint publication year: 2008
References
, , , and (1995). A comparison of the effects of anterior thalamic, mamillary body and fornix lesions on reinforced spatial alternation. Behav Brain Res 68:91–101.CrossRefGoogle ScholarPubMed
, , , and (1979). Septo-hippocampal pathway necessary for dentate theta production. Brain Res 165:13–22.CrossRefGoogle ScholarPubMed
and (2001). Hippocampal theta oscillations and classical conditioning. Neurobiol Learn Mem 76:298–313.CrossRefGoogle ScholarPubMed
and (1978). Prediction of learning rate from the hippocampal electroencephalogram. Science 200:1298–1300.CrossRefGoogle ScholarPubMed
and (1998). Synaptic modifications in cultured hippocampal neurons: dependence on spike timing, synaptic strength, and postsynaptic cell type. J Neurosci 18:10 464–10 472.CrossRefGoogle ScholarPubMed
and (1993). A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361:31–39.CrossRefGoogle ScholarPubMed
and (1973). Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path. J Physiol 232:331–356.CrossRefGoogle ScholarPubMed
and (2003). Cellular mechanisms underlying the rhythmic bursts induced by NMDA microiontophoresis at the apical dendrites of CA1 pyramidal neurons. Hippocampus 13:150–163.CrossRefGoogle ScholarPubMed
, , and (1978). Reset of hippocampal rhythmical activities by afferent stimulation. Brain Res Bull 3:21–28.CrossRefGoogle ScholarPubMed
, , and (1983). Cellular bases of hippocampal EEG in the behaving rat. Brain Res 287:139–171.CrossRefGoogle ScholarPubMed
, , , and (1986). Laminar distribution of hippocampal rhythmic slow activity (RSA) in the behaving rat: current-source density analysis, effects of urethane and atropine. Brain Res 365:125–137.CrossRefGoogle ScholarPubMed
, , , and (2001). An experimental test of the role of postsynaptic calcium levels in determining synaptic strength using perirhinal cortex of rat. J Physiol 532:459–466.CrossRefGoogle ScholarPubMed
, , and (1983). Excitatory amino acids in synaptic transmission in the Schaffer collateral–commissural pathway of the rat hippocampus. J Physiol 3:33–46.CrossRefGoogle Scholar
, , and (2001). Bidirectional synaptic plasticity correlated with the magnitude of dendritic calcium transients above a threshold. J Neurophysiol 85:399–406.CrossRefGoogle ScholarPubMed
, , and (1996). Calcium-dependent paired-pulse facilitation of miniature EPSC frequency accompanies depression of EPSCs at hippocampal synapses in culture. J Neurosci 16:5312–5322.CrossRefGoogle ScholarPubMed
and (1994). Stress impairs LTP and hippocampal-dependent memory. Ann N Y Acad Sci 746:411–414.CrossRefGoogle ScholarPubMed
and (1993). Bidirectional long-term modification of synaptic effectiveness of adult and immature hippocampus. J Neurosci 13:2190–2198.CrossRefGoogle ScholarPubMed
and (1979). The relationship between extracellular calcium concentrations and the induction of hippocampal long-term potentiation. Brain Res 169:103–110.CrossRefGoogle ScholarPubMed
(2000). A cortical–hippocampal system for declarative memory. Nat Rev Neurosci 1:41–50.CrossRefGoogle ScholarPubMed
, , , and (1987). Cue-sampling and goal-approach correlates of hippocampal unit activity in rats performing an odor-discrimination task. J Neurosci 7:716–732.CrossRefGoogle ScholarPubMed
, , and (1996). Neurotoxic lesions of the perirhinal cortex do not mimic the behavioural effects of fornix transection in the rat. Behav Brain Res 80:9–25.CrossRefGoogle Scholar
, , and (1986). Hippocampal theta rhythm and the firing of neurons in walking and urethane anesthetized rats. Brain Res 62:495–508.Google ScholarPubMed
(1996). Stimulus-evoked resetting of the dentate theta rhythm: relation to working memory. Neuroreport 8:159–163.CrossRefGoogle ScholarPubMed
and (1990). Cholinergic and GABAergic modulation of the medial septal area: effect on working memory. Behav Neurosci 104:849–855.CrossRefGoogle ScholarPubMed
and (1994). Local modulation of basal forebrain: effects on working and reference memory. J Neurosci 14:3578–3587.CrossRefGoogle ScholarPubMed
, , and (2002). Dendritic spikes as a mechanism for cooperative long-term potentiation. Nature 418:326–331.CrossRefGoogle Scholar
, , and (2005). A model of STDP based on spatially and temporally local information: derivation and combination with gated decay. Neur Networks 18:458–466.CrossRefGoogle ScholarPubMed
and (1954). Hippocampal electrical activity and arousal. J Neurophysiol 17:533–557.CrossRefGoogle ScholarPubMed
, , and (1988). Long-term potentiation in the dentate gyrus is preferentially induced at theta rhythm periodicity. Brain Res 438:331–334.CrossRefGoogle ScholarPubMed
, , , and (2004). Theta-contingent trial presentation accelerates learning rate and enhances hippocampal plasticity during trace eyeblink conditioning. Behav Neurosci 118:403–411.CrossRefGoogle ScholarPubMed
and (2005). Hippocampal mechanisms for the context-dependent retrieval of episodes. Neur Networks 15:689–707.CrossRefGoogle Scholar
, , and (2002). A proposed function for hippocampal theta rhythm: separate phases of encoding and retrieval enhance reversal of prior learning. Neur Comput 14:793–817.CrossRefGoogle ScholarPubMed
(1949). The Organization of Behavior: A Neuropsychological Theory. New York: John Wiley.Google Scholar
, , and (1997). 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. J Neurosci 17:6470–6477.CrossRefGoogle ScholarPubMed
and (1995). Bidirectional synaptic plasticity induced by a single burst during cholinergic theta oscillation in CA1 in vitro. Neuron 15:1053–1063.CrossRefGoogle ScholarPubMed
, , and (2003). Independent rate and temporal coding in hippocampal pyramidal cells. Nature 425:828–832.CrossRefGoogle ScholarPubMed
, , , , and (2003). 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. J Neurosci 23:11 725–11 731.CrossRefGoogle ScholarPubMed
and (1987). Glutamate activates multiple single channel conductances in hippocampal neurons. Nature 325:522–525.CrossRefGoogle ScholarPubMed
, , , and (1998). Theta oscillations in somata and dendrites of hippocampal pyramidal cells in vivo: activity-dependent phase-precession of action potentials. Hippocampus 8:244–261.3.0.CO;2-J>CrossRefGoogle ScholarPubMed
, , and (2002). Mechanisms and significance of spike-timing dependent plasticity. Biol Cybern 87:373–382.CrossRefGoogle ScholarPubMed
and (1998). Calcium dynamics in single spines during coincident pre- and postsynaptic activity depend on relative timing of back-propagating action potentials and subthreshold excitatory postsynaptic potentials. Proc Natl Acad Sci USA 95:9596–9601.CrossRefGoogle ScholarPubMed
and (1986). Induction of synaptic potentiation in hippocampus by patterned stimulation involves two events. Science 232:985–988.CrossRefGoogle ScholarPubMed
(1989). A mechanism for the Hebb and the anti-Hebb processes underlying learning and memory. Proc Natl Acad Sci USA 86:9574–9578.CrossRefGoogle ScholarPubMed
(2001). Three Ca2+ levels affect plasticity differently: the LTP zone, the LTD zone and no man's land. J Physiol 532:285.CrossRefGoogle ScholarPubMed
, , , , and (1983). Intracellular injections of EGTA block induction of hippocampal long-term potentiation. Nature 305:719–721.CrossRefGoogle ScholarPubMed
, , , and (1989). A comparative analysis of the role of fornix and cingulate cortex in memory: rats. Exp Brain Res 74:187–201.CrossRefGoogle ScholarPubMed
, , , and (2004). Theta reset produces optimal conditions for long-term potentiation. Hippocampus 14:684–687.CrossRefGoogle ScholarPubMed
, , , et al. (1987). Effects of selective lesions of fimbria-fornix on learning set in the rat. Physiol Behav 40:181–188.CrossRefGoogle ScholarPubMed
(1978). Memory in monkeys severely impaired by combined but not by separate removal of amygdala and hippocampus. Nature 273:297–298.CrossRefGoogle Scholar
, , , and (1982). Place navigation impaired in rats with hippocampal lesions. Nature 297:681–683.CrossRefGoogle ScholarPubMed
and (1992). Mechanisms underlying induction of homosynaptic long-term depression in area CA1 of the hippocampus. Neuron 9:967–975.CrossRefGoogle ScholarPubMed
and (1990). Effects of medial septal lesions on operant delayed alternation in rats. Brain Res 531:232–241.CrossRefGoogle ScholarPubMed
and (1978). Hippocampal place units in the freely moving rat: why they fire where they fire. Exp Brain Res 31:573–590.CrossRefGoogle ScholarPubMed
and (1971). The hippocampus as a spatial map: preliminary evidence from unit activity in the freely-moving rat. Brain Res 34:171–175.CrossRefGoogle ScholarPubMed
and (1993). Phase relationship between hippocampal place units and the EEG theta rhythm. Hippocampus 3:317–330.CrossRefGoogle ScholarPubMed
, , , , and (2001). Hippocampal synaptic plasticity is modulated by theta rhythm in the fascia dentata of adult and aged freely behaving rats. Hippocampus 11:647–654.CrossRefGoogle ScholarPubMed
, , , and (1988). Long-term potentiation in the dentate gyrus is induced preferentially on the positive phase of theta-rhythm. Brain Res 439:383–387.CrossRefGoogle ScholarPubMed
, , and (1979). Septo-hippocampal connections and the hippocampal theta rhythm. Exp Brain Res 37:49–63.CrossRefGoogle ScholarPubMed
, , , et al. (2003). Reset of human neocortical oscillations during a working memory task. Proc Natl Acad Sci USA 100:7931–7936.CrossRefGoogle ScholarPubMed
, , , and (2005). Calcium time course as a signal for spike-timing-dependent plasticity. J Neurophysiol 93:2600–2613.CrossRefGoogle ScholarPubMed
and (1957). Loss of recent memory after bilateral hippocampal lesions. J Neurol Neurosurg Psychiat 20:11–21.CrossRefGoogle ScholarPubMed
, , , , and (2002). Oscillatory brain states and learning: impact of hippocampal theta-contingent training. Proc Natl Acad Sci USA 99:1616–1620.CrossRefGoogle ScholarPubMed
and (1996). Replay of neuronal firing sequences in rat hippocampus during sleep following spatial experience. Science 271:1870–1873.CrossRefGoogle ScholarPubMed
, , , and (1996). Theta phase precession in hippocampal neuronal populations and the compression of temporal sequences. Hippocampus 6:149–172.3.0.CO;2-K>CrossRefGoogle ScholarPubMed
(1996). LTD, LTP, and the sliding threshold for long-term synaptic plasticity. Hippocampus 6:35–42.3.0.CO;2-6>CrossRefGoogle ScholarPubMed
, , , and (1992). Firing relations of medial entorhinal neurons to the hippocampal theta rhythm in urethane anesthetized and walking rats. Exp Brain Res 90:21–28.CrossRefGoogle ScholarPubMed
(1968). Recovery from large medial thalamic lesions as a result of electroconvulsive therapy. J Neurol Neurosurg Psychiat 31:67–72.CrossRefGoogle ScholarPubMed
(1971). Limbic–diencephalic mechanisms of voluntary movement. Psychol Rev 78:83–113.CrossRefGoogle ScholarPubMed
(1975). Neocortical and hippocampal activation relation to behavior: effects of atropine, eserine, phenothiazines, and amphetamine. J Comp Physiol Psychol 88:300–323.CrossRefGoogle ScholarPubMed
and (1997). Brainstem–diencephalo-septohippocampal systems controlling the theta rhythm of the hippocampus. Neuroscience 81:893–926.Google ScholarPubMed
, , , and (2005). Coactivation and timing-dependent integration of synaptic potentiation and depression. Nat Neurosci 8:187–193.CrossRefGoogle ScholarPubMed
and (1997). Perseveration on place reversals in spatial swimming pool tasks: further evidence for place learning in hippocampal rats. Hippocampus 7:361–370.3.0.CO;2-M>CrossRefGoogle ScholarPubMed
(1978). Loss of hippocampal theta rhythm results in spatial memory deficit in the rat. Science 201:160–163.CrossRefGoogle ScholarPubMed
and (2006). Malleability of spike-timing-dependent plasticity at the CA3–CA1 synapse. J Neurosci 26:6610–6617.CrossRefGoogle ScholarPubMed
, , and (1999). Selective induction of LTP and LTD by postsynaptic [Ca2+]i elevation. J Neurophysiol 81:781–787.CrossRefGoogle ScholarPubMed
, , , et al. (1995). Intracellular correlates of hippocampal theta rhythm in identified pyramidal cells, granule cells, and basket cells. Hippocampus 5:78–90.CrossRefGoogle ScholarPubMed