Locus coeruleus potentiation of dentate gyrus responses: Evidence for two systems

Harley, Carolyn W.; Milway, J. Stephen; Lacaille, Jean‐Claude

doi:10.1016/0361-9230(89)90084-1

Cited by 55 publications

(34 citation statements)

References 30 publications

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“…The early effects of LC activation parallel those reported in other studies (Lacaille and Harley, 1985;Harley et al, 1989;Washburn and Moises, 1989;Klukowski and Harley, 1994) and suggest that there may be both short-term and intermediate forms of NE potentiation. There is some evidence presented here that the site of LC activation (cerulear vs pericerulear) influences short-and intermediate-term effects on the evoked activity.…”

Section: Discussionsupporting

confidence: 83%

“…This suggests the LC mechanism supports long-term, but not short-term, memory. Thus, glutamate infusion in the LC, known to produce a burst of LC cell activity (Harley and Sara, 1992), may initially promote spike potentiation, as seen here and in previous studies (Harley and Milway, 1986;Harley et al, 1989;Washburn and Moises, 1989); however, a significant increase in EPSP slope is observed 24 hr later. The increase in EPSP slope at 24 hr predicts the increase in population spike amplitude at that time.…”

Section: Discussionsupporting

confidence: 79%

“…In in vivo studies using anesthetized rats, norepinephrine, or activation of the LC, increases granule cell excitability, as indexed by larger population spikes to perforant path stimulation, without increasing synaptic strength, as indexed by EPSP slope (Neuman and Harley, 1983;Harley and Milway, 1986;Harley et al, 1989).…”

Section: Introductionmentioning

confidence: 99%

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Locus Ceruleus Activation Initiates Delayed Synaptic Potentiation of Perforant Path Input to the Dentate Gyrus in Awake Rats: A Novel β-Adrenergic- and Protein Synthesis-Dependent Mammalian Plasticity Mechanism

Walling¹,

Harley²

2004

J. Neurosci.

102

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Norepinephrine, acting through ␤-adrenergic receptors, is implicated in mammalian memory. In in vitro and in vivo studies, norepinephrine produces potentiation of the perforant path-dentate gyrus evoked potential; however, the duration and dynamics of norepinephrine-induced potentiation have not been explored over extended time periods. To characterize the long-term effects of norepinephrine on granule cell plasticity, the present study uses glutamatergic activation of the locus ceruleus (LC) to induce release of norepinephrine in the hippocampus of the awake rat and examines the subsequent modulation of the dentate gyrus evoked potential for 3 hr (short term) and 24 hr (long term) after LC activation. LC activation initiates a potentiation of the field EPSP slope observed 24 hr later. This late-phase potentiation of the synaptic potential is not preceded by early phase potentiation, although spike potentiation can be seen both immediately after, and 24 hr after, LC activation. Intracerebroventricular infusion of the ␤-adrenergic antagonist, propranolol, or the protein synthesis inhibitor, anisomycin, before LC activation blocks the potentiation of perforant path input observed at 24 hr. The initiation of late-phase synaptic potentiation observed at 24 hr but not at the 3 hr after LC activation parallels the observation of a cAMP-and protein synthesis-dependent long-lasting synaptic facilitation in Aplysia that is not preceded by shortterm synaptic facilitation. Locus ceruleus-initiated synaptic potentiation may selectively support long-term, rather than short-term, memory. The observation of selective initiation of long-term synaptic facilitation in a mammalian brain, as in invertebrates, is additional evidence that these two forms of memory depend on separable biological mechanisms.

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Section: Discussionsupporting

confidence: 83%

Section: Discussionsupporting

confidence: 79%

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Locus Ceruleus Activation Initiates Delayed Synaptic Potentiation of Perforant Path Input to the Dentate Gyrus in Awake Rats: A Novel β-Adrenergic- and Protein Synthesis-Dependent Mammalian Plasticity Mechanism

Walling¹,

Harley²

2004

J. Neurosci.

102

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“…The use of electrical stimulation may be another source of difference in outcome, because electrical stimulation in the locus ceruleus area can produce effects not dependent on noradrenergic mediation (Harley et al, 1989;Branchereau et al, 1996). Intracellular recordings of identified granule cells after exogenous norepinephrine reveal a modest depolarization (Lacaille and Schwartzkroin, 1988).…”

Section: Discussionmentioning

confidence: 99%

Locus Ceruleus Activation Suppresses Feedforward Interneurons and Reduces β-γ Electroencephalogram Frequencies While It Enhances θ Frequencies in Rat Dentate Gyrus

Brown¹,

Walling²,

Milway³

et al. 2005

J. Neurosci.

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The locus ceruleus is activated by novel stimuli, and its activation promotes learning and memory. Phasic activation of locus ceruleus neurons by glutamate enhances the dentate gyrus population spike amplitude and results in long-term potentiation of synaptic responses recorded after 24 h. Cholinergic activation of locus ceruleus neurons increases hippocampal . At the level of the cellular network, it is not clear how the potentiating effects of norepinephrine are mediated. Previous studies show that exogenous norepinephrine enhances inhibitory interneuron firing in the dentate gyrus. This finding appears at odds with evidence for potentiation. In this study, natural release of norepinephrine was induced by glutamate activation of locus ceruleus while we recorded EEGs and physiologically identified interneurons in the dentate gyrus of urethane-anesthetized rats. Feedforward neurons were inhibited (ϳ1-2 min) by locus ceruleus activation. Feedback interneurons showed both increased and decreased activity, whereas granule cells increased firing as predicted by evoked potential studies. EEG results replicated an increase in power (4 -8 Hz) with locus ceruleus activation, but the effect with glutamatergic locus ceruleus activation was transient (ϳ1-2 min). ␤-␥ Frequencies were also transiently suppressed. Together, the data suggest that locus ceruleus activation enhances the throughput of concomitant sensory input by reducing feedforward inhibitory interneuron activity, which may reduce "binding" in existing cell assemblies, and enhances the conditions for synaptic plasticity through disinhibition, promotion of 4 -8 Hz , and noradrenergic potentiation to facilitate the building of new representations.

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“…See Sara (2009) for a comprehensive review of current theories of LC function and timeline of discoveries. With respect to a role in synaptic plasticity, norepinephrine (NE) released from the LC by glutamatergic activation, produces a protein synthesis-and b-adrenergic receptordependent potentiation in the dentate gyrus of the hippocampus (Harley and Milway, 1986;Harley et al, 1989;. Taken together, this information suggests that NE released from the LC may serve as an important modulating signal for the integration of external sensory information, top-down signaling and memory processing.…”

Section: Introductionmentioning

confidence: 96%

Selective tuning of hippocampal oscillations by phasic locus coeruleus activation in awake male rats

et al. 2011

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Theta and gamma oscillations are thought to provide signal sets that promote neural coding of cognitive processes. Over 40 yrs ago, Jeffrey Gray reported event-related changes in a narrow band of hippocampal theta (7.5-8.5 Hz) which appeared to involve norepinephrine (NE) release from, the noradrenergic nucleus, the locus coeruleus (LC). These event-related alterations in EEG were elicited by novelty, attentional changes, the use of preparatory signals, and signal-mismatch events. Gray et al. have since provided indirect evidence that supports the role of NE in the modulation of 7.5- to 8.5-Hz oscillations in the hippocampus, but studies investigating the effects of direct LC activation in awake rats have been lacking. In the present study, dentate gyrus EEG was examined during glutamatergic activation of the LC in awake male rats in relation to plasticity effects on simultaneously recorded perforant path-evoked field potentials. Glutamate-injected animals were divided into three groups based on histological and plasticity outcomes; perforant path stimulated controls were also included. The three injected groups were: (1) rats with positive LC placements, demonstrating NE-LTP of the dentate gyrus evoked potential, (2) rats with positive LC placements, without NE-LTP, and (3) Non-LC injected controls. Activation of the LC in awake rats demonstrating NE-LTP increased the relative power of 7- to 9-Hz theta, a result masked in broader 4- to 12-Hz analysis. Comparatively, urethane-anesthetized rats showed an increase in 5-7 Hz, but not 7- to 9-Hz theta with LC activation. Discriminative analysis in the approximate theta band predicted by Gray (7.4-8.5 Hz) revealed that awake rats demonstrating NE-LTP had increased relative power in this narrow frequency compared to rats receiving perforant path only (noninjected) and Non-LC injected rats. Transiently reduced gamma (20-40 Hz) relative power was most commonly observed in rats with verified LC placements failing to express NE-LTP. Given current theories of LC function, these results suggest oscillatory tuning within the theta and gamma range may facilitate shifts in cognitive set.

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Locus coeruleus potentiation of dentate gyrus responses: Evidence for two systems

Cited by 55 publications

References 30 publications

Locus Ceruleus Activation Initiates Delayed Synaptic Potentiation of Perforant Path Input to the Dentate Gyrus in Awake Rats: A Novel β-Adrenergic- and Protein Synthesis-Dependent Mammalian Plasticity Mechanism

Locus Ceruleus Activation Initiates Delayed Synaptic Potentiation of Perforant Path Input to the Dentate Gyrus in Awake Rats: A Novel β-Adrenergic- and Protein Synthesis-Dependent Mammalian Plasticity Mechanism

Locus Ceruleus Activation Suppresses Feedforward Interneurons and Reduces β-γ Electroencephalogram Frequencies While It Enhances θ Frequencies in Rat Dentate Gyrus

Selective tuning of hippocampal oscillations by phasic locus coeruleus activation in awake male rats

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