Estimating the synaptic concentration of norepinephrine in dentate gyrus which produces β-receptor mediated long-lasting potentiation in vivo using microdialysis and intracerebroventricular norepinephrine

Harley, Carolyn W.; Lalies, Margaret D.; Nutt, David

doi:10.1016/0006-8993(95)01443-8

Cited by 37 publications

(34 citation statements)

References 26 publications

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“…Specifically, similarly to neonates, neural correlates of learning could be achieved by large NE infusions directly into the olfactory bulb, hippocampus, and auditory cortex of the adult rat, suggesting that the mature brain retains at least some potential for NE-dependent plasticity, provided that sufficient levels of NE are available (Gray et al, 1986;Harley et al, 1996;Chaulk and Harley, 1998;Harley, 1998;Edeline, 1999).…”

Section: Discussionmentioning

confidence: 99%

Unique Neural Circuitry for Neonatal Olfactory Learning

Moriceau¹,

Sullivan²

2004

J. Neurosci.

129

112

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Imprinting ensures that the infant forms the caregiver attachment necessary for altricial species survival. In our mammalian model of imprinting, neonatal rats rapidly learn the odor-based maternal attachment. This rapid learning requires reward-evoked locus ceruleus (LC) release of copious amounts of norepinephrine (NE) into the olfactory bulb. This imprinting ends at postnatal day 10 (P10) and is associated with a dramatic reduction in reward-evoked LC NE release. Here we assess whether the functional emergence of LC ␣2 inhibitory autoreceptors and the downregulation of LC ␣1 excitatory autoreceptors underlie the dramatic reduction in NE release associated with termination of the sensitive period. Postsensitive period pups (P12) were implanted with either LC or olfactory bulb cannulas, classically conditioned with intracranial drug infusions (P14), and tested for an odor preference (P15). During conditioning, a novel odor was paired with either olfactory bulb infusion of a ␤-receptor agonist (isoproterenol) to assess the target effects of NE or direct LC cholinergic stimulation combined with ␣2 antagonists and ␣1 agonists in a mixture to reinstate neonatal levels of LC autoreceptor activity to assess the source of NE. Pups learned an odor preference when the odor was paired with either olfactory bulb isoproterenol infusion or reinstatement of neonatal LC receptor activity. These results suggest that LC autoreceptor functional changes rather than olfactory bulb changes underlie sensitive period termination.

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Section: Discussionmentioning

confidence: 99%

Unique Neural Circuitry for Neonatal Olfactory Learning

Moriceau¹,

Sullivan²

2004

J. Neurosci.

129

112

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“…After ORX-A infusion into the LC, sampling continued until NE returned to baseline. Analysis of NE was performed by means of HPLC with electrochemical detection (Harley et al, 1996). In brief, the mobile phase was prepared using a stock mixture of 24 mM sodium acetate, 15 mM citric acid, and 2.3 mM octane-sulfonic acid in deionized water, to which methanol (13% v/v) was added.…”

Section: Microdialysis Experimentsmentioning

confidence: 99%

“…NE diasylate in the hippocampus was obtained using a concentric dialysis probe constructed as described by Harley et al (1996), but using a 4 mm exposed membrane. The larger probe provided a more stable sample of NE levels.…”

Section: Microdialysis Experimentsmentioning

confidence: 99%

Orexin-A Infusion in the Locus Ceruleus Triggers Norepinephrine (NE) Release and NE-Induced Long-Term Potentiation in the Dentate Gyrus

Walling¹,

Nutt²,

Lalies³

et al. 2004

J. Neurosci.

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The orexins (ORX-A/ORX-B) are neuroactive peptides known to have roles in feeding and sleep. Evidence of dense, excitatory projections of ORX-A neurons to the noradrenergic pontine nucleus, the locus ceruleus (LC), suggests ORX-A also participates in attention and memory. Activation of LC neurons by glutamate produces a ␤-adrenergic receptor-mediated long-term potentiation (LTP) of the perforant path-evoked potential in the dentate gyrus, a target structure of the LC that has been implicated in memory. We asked whether ORX-A also activates norepinephrine (NE)-induced LTP by initiating NE release in the hippocampus. Here, we show that ORX-A infusion (0.25-25 fmol) into the LC produces a robust, ␤-adrenergic receptor-dependent, long-lasting potentiation of the perforant path-evoked dentate gyrus population spike in the anesthetized rat. Pharmacological inactivation of the LC with an ␣ 2 -adrenergic receptor agonist, before ORX-A infusion, prevents this potentiation. Analysis of NE concentrations in the hippocampus after ORX-A infusion into the LC reveals a transient, but robust, increase in NE release. Thus, this study demonstrates that the dense orexinergic projection to the LC promotes the induction of NE-LTP in the dentate gyrus. ORX-A modulation of LC activity may provide important support for the cognitive processes of attention and memory.

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“…Second, excitatory compounds can produce inactivation depolarization (Adams and Foote, 1988) which may cause NE release failure in some animals. Lastly, although every attempt was made to ensure a complete glutamate injection, differences may have existed in the total volume displaced into the LC, and thus either the number of cells recruited, and amount of NE released in the hippocampus, may have been subthreshold to initiate potentiation of the evoked response (Harley et al, 1996) and/or network oscillations.…”

Section: Glutamate Activation Of the Lc Selectively Increases The Relmentioning

confidence: 99%

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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Estimating the synaptic concentration of norepinephrine in dentate gyrus which produces β-receptor mediated long-lasting potentiation in vivo using microdialysis and intracerebroventricular norepinephrine

Cited by 37 publications

References 26 publications

Unique Neural Circuitry for Neonatal Olfactory Learning

Unique Neural Circuitry for Neonatal Olfactory Learning

Orexin-A Infusion in the Locus Ceruleus Triggers Norepinephrine (NE) Release and NE-Induced Long-Term Potentiation in the Dentate Gyrus

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

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