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Postnatal development of electrical activity in the locus ceruleus
Abstract
1. A method for adapting a standard stereotaxic frame for use with neonatal rats as young as postnatal day 1 (PD 1) was devised, and single-unit extracellular recordings were obtained from neurons in the locus ceruleus (LC) in urethan-anesthetized rats during different stages in development from PD 1 to PD 34. 2. The spontaneous firing pattern of neonatal LC neurons was characterized by long silent periods punctuated by brief epochs of sporadic firing. At PD 7-14, LC neurons exhibited periodic occurrences of irregular firing that lasted for 20-30 s. By PD 20, the pattern and rate of spontaneous activity were virtually indistinguishable from that of adults. 3. Conditioning stimulation of the dorsal noradrenergic bundle (DNB), given 10-200 ms prior to a test stimulus to the DNB, markedly reduced the amplitude of the antidromic action potentials to the test stimulus and sometimes resulted in spike decomposition. This refractoriness of the soma-dendritic membrane of LC cells was significantly attenuated with development and approached adult levels after PD 18. 4. Antidromic responses elicited by DNB stimulation were followed by a phase of inhibition or inhibition-excitation. Postactivation excitation was most prominent in cells that were not spontaneously active, and decreased steadily throughout development, probably because of the steady increase in spontaneous firing rate seen during maturation. 5. Although the conduction velocity of LC axons increased steadily from birth through PD 26, conduction time remained unchanged. 6. Neonatal LC neurons were equally sensitive to noxious and nonnoxious somatosensory stimuli. As development proceeded, LC neurons became less sensitive to innocuous somatosensory stimuli such as air puffs and tactile stimuli while simultaneously becoming more sensitive to noxious stimuli. Auditory and visual stimuli became effective for the first time at PD 14 and PD 12, respectively. 7. These results indicate that the electrical activity of LC neurons in the developing brain is intimately related to input from peripheral sensory sources. Therefore, the influence of the LC on the developing brain may occur predominantly through sensory input.
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“In particular, the large amounts of NE required for this attachment-related plasticity results from the failure of the infant LC to show habituation or to turn itself off via auto-inhibition (as occurs in older pups and adults) (Nakamura et al., 1987, Winzer-Serhan et al., 1996).”
From Early life adversity during the infant sensitive period for attachment: Programming of behavioral neurobiology of threat processing and social behavior (2017) · cites this paper as Nakamura et al., 1987
In the citing paper
“The mechanism for the prolonged neonatal LC response appears due to the lack of functional α2 inhibitory noradrenergic autoreceptors that terminate the LC response in older pups/adult (Nakamura et al., 1987; Pieribone et al., 1994; Scheinin et al., 1994; Winzer-Serhan et al., 1999).”
From Early-life stress disrupts attachment learning: the role of amygdala corticosterone, locus ceruleus corticotropin releasing hormone, and olfactory bulb norepinephrine (2009) · cites this paper as Nakamura et al., 1987
In the citing paper
“In contrast, in older pups and adult, the LC has different characteristics limiting NE release that is associated with α2 inhibitiory autoreceptors functional emergence (Nakamura et al., 1987; Nakamura and Sakaguchi, 1990; Scheinin et al., 1994).”
From Early-life stress disrupts attachment learning: the role of amygdala corticosterone, locus ceruleus corticotropin releasing hormone, and olfactory bulb norepinephrine (2009) · cites this paper as Nakamura et al., 1987
In the citing paper
“Indeed, developmental differences in LC activity are reflected during both noxious (electric shock) and nonnoxious (stroking) stimulus-evoked NE release in the olfactory bulb, with neonatal pups releasing significantly more NE than older pups/adult (Kimura and Nakamura, 1987; Nakamura et al., 1987; Nakamura and Sakaguchi, 1990; McLean and Shipley, 1991; Sullivan et al., 1992; Sullivan and Wilson,”
From Early-life stress disrupts attachment learning: the role of amygdala corticosterone, locus ceruleus corticotropin releasing hormone, and olfactory bulb norepinephrine (2009) · cites this paper as Nakamura et al., 1987
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Locus coeruleus: a new look at the blue spot
Poe, G. R., Foote, S., Eschenko, O., Johansen, J. P., Bouret, S., Aston-Jones, G., Harley, C. W., Manahan-Vaughan, D., Weinshenker, D., Valentino, R., et al. (2020) · Nature Reviews Neuroscience · doi:10.1038/s41583-020-0360-9 · Cited by 720
Norepinephrine and learning-induced plasticity in infant rat olfactory system
Sullivan, R., Wilson, D., & Leon, M. (1989) · The Journal of Neuroscience · doi:10.1523/jneurosci.09-11-03998.1989 · Cited by 261
“Isoproterenol is an exogenous source of NE which acts upon NE P-receptors to mimic the action of NE. Stroking may evoke a rise in endogenous NE, since stroking activates locus coeruleus neurons in infant rats (Nakamura et al., 1987).”
BackgroundMoriceau, S., Shionoya, K., Jakubs, K., & Sullivan, R. M. (2009) · The Journal of Neuroscience · doi:10.1523/jneurosci.4106-09.2009 · Cited by 214
“shock) and non-noxious (stroking) stimulus-evoked NE release in the olfactory bulb, with neonatal pups releasing significantly more NE than older pups/adult (Kimura and Nakamura, 1987; Nakamura et al., 1987; Nakamura and Sakaguchi, 1990; McLean and Shipley, 1991; Sullivan et al., 1992, 2000b; Sullivan and Wilson, 1994…”
BackgroundNeurobiology of associative learning in the neonate: Early olfactory learning
Wilson, D. A., & Sullivan, R. M. (1994) · Behavioral and Neural Biology · doi:10.1016/s0163-1047(05)80039-1 · Cited by 206
Tepper, J. M., Sharpe, N. A., Koós, T. Z., & Trent, F. (1998) · Developmental Neuroscience · doi:10.1159/000017308 · Cited by 194
“…potentials recorded in other brain regions of neonatal rats including hippocampus, neocortex, substantia nigra, and locus ceruleus [e.g., Fukuda and Prince, 1992; Lorenzon and Foehring, 1993; McCormick and Prince, 1987; Nakamura et al., 1987; Tepper et al., 1990; Williams and Marshall, 1987].”
Background
Metadata
- Authors
- Nakamura, S., Kimura, F., & Sakaguchi, T.
- Affiliations
- The University of Osaka (JP)
- Venue
- Journal of Neurophysiology
- Publisher
- American Physiological Society
- Published
- 1987-09-01
- Volume
- 58
- Issue
- 3
- Pages
- 510-524
- ISSN
- 0022-3077 (ISSN-L)
- 1522-1598
- OpenAlex
- W2412072574
- Cited by
- 130
- References
- 0
- Citations by year
- 2026: 2 · 2025: 3 · 2023: 4 · 2022: 3 · 2021: 1 · 2020: 4 · 2019: 2 · 2018: 2 · 2017: 6 · 2016: 6 · 2015: 2 · 2014: 9 · 2013: 2 · 2012: 7
- FWCI
- 1.25
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Journal of Neurophysiology (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Neuroscience of respiration and sleep
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Keywords
- locus coeruleus, postnatal development, spontaneous firing, neonatal rats, antidromic action potentials, dorsal noradrenergic bundle, sensory input, axonal conduction velocity, noradrenergic neurons
- MeSH terms
- Aging, Animals, Animals, Newborn, Electrophysiology, Locus Coeruleus, Neurons, Rats, Inbred Strains, Rats
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