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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The large amounts of NE required for attachment-related plasticity result from the failure of the infant LC to show habituation or to turn itself off via auto-inhibition.
“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
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.
“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 older pups and adult, the LC has different characteristics limiting NE release that is associated with α2 inhibitory autoreceptors functional emergence.
“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
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.
“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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“This latency is similar to the 4-to 5-msec latency shown by Nicoll (1972) in vivo, in rabbit, using a 1-to 2-mm stimulating-to-recording separation with ON conduction velocity estimated at 0.34 m/sec.”
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“For example, the noradrenergic locus ceruleus, which is activated by arousing stimuli, is more easily excited during development than in adulthood, and its activation is longer lasting, as well (Nakamura et al., 1987 ) .”
BackgroundA temporal-specific and transient cAMP increase characterizes odorant classical conditioningPreprint
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“NE is released from the locus coeruleus (LC) following tactile stimulation (Nakamura et al., 1987; Nakamura and Sakaguchi, 1990; Rangel and Leon, 1995) and pharmacological blocking of either α- or β-adrenoceptors in the olfactory bulb (OB; Sullivan et al., 2000b; Shakhawat et al., 2012), or the…”
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Paladini, C. A., Beckstead, M. J., & Weinshenker, D. (2006) · Neuroscience · doi:10.1016/j.neuroscience.2006.10.032 · Cited by 18 · see citing works
“Furthermore, the firing patterns of LC neurons in vivo also change during this time period (Nakamura et al., 1987).”
BackgroundJerome, D. K., Hou, Q., & Yuan, Q. (2012) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2012.08210.x · Cited by 17 · see citing works
“Stroking stimulates locus coeruleus neurons in the rat, which release norepinephrine into the olfactory bulb (Nakamura et al., 1987). bAdrenoceptor activation in the olfactory bulb has been shown to be sufficient as a substitute for natural norepinephrine release to induce odor preference learning…”
BackgroundWang, Y.-J., Okutani, F., Murata, Y., Taniguchi, M., Namba, T., & Kaba, H. (2012) · Neuroscience · doi:10.1016/j.neuroscience.2012.12.015 · Cited by 17 · see citing works
“projection originating from the locus coeruleus (Nakamura et al., 1987).”
BackgroundOhshima, M., Itami, C., & Kimura, F. (2017) · The Journal of Physiology · doi:10.1113/jp275142 · Cited by 16 · see citing works
“…classically including arousal, attention and the sleep–wake cycle, and play a more complex and specific role in the regulation of behaviour (Berridge & Waterhouse, 2003; Aston-Jones & Cohen, 2005) throughout animals’ lives (Nakamura et al. 1987) from neonates (Kimura & Nakamura, 1985, 1987).”
BackgroundSelf-citationAmygdala circuit transitions supporting developmentally-appropriate social behavior
Ferrara, N. C., & Opendak, M. M. (2023) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2023.107762 · Cited by 17 · see citing works
GABAergic inhibitory response of locus coeruleus neurons to caloric vestibular stimulation in rats
Nishiike, S., Nakamura, S., Arakawa, S., Takeda, N., & Kubo, T. (1996) · Brain Research · doi:10.1016/0006-8993(95)01485-3 · Cited by 14 · see citing works
Self-citationMcLean, J. H., Smith, A. L., Rogers, S., Clarke, K., Darby‐King, A., & Harley, C. W. (2009) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2009.02.003 · Cited by 13 · see citing works
Seifi, M., Corteen, N. L., van der Want, J. J. L., Metzger, F., & Swinny, J. D. (2014) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2014.00031 · Cited by 13 · see citing works
“Adult NG2 cells are distributed in both gray and white matter regions of the brain (Nishiyama et al.,1999), are in synaptic contact with neurons (Bergles et al., 2000; Ge et al., 2006) and proliferate Frontiers in Neuroanatomy www.frontiersin.org May 2014 | Volume 8 | Article 31 | 1 in response to…”
BackgroundFetal Alcohol Syndrome: Early Olfactory Learning as a Model System to Study Neurobehavioral Deficits
Kirstein, C. L., Philpot, R. M., & Dark, T. (1997) · International Journal of Neuroscience · doi:10.3109/00207459708988467 · Cited by 13 · see citing works
O’Leary, K. T., & Leslie, F. M. (2005) · Neuropharmacology · doi:10.1016/j.neuropharm.2005.08.013 · Cited by 13 · see citing works
Aoki, C. J. (1997) · Visual Neuroscience · doi:10.1017/s0952523800011822 · Cited by 13 · see citing works
Air-stepping in neonatal rats: A comparison of L-dopa injection and olfactory stimulation.
Jamon, M., Maloum, I., Riviere, G., et al. (2002) · Behavioral Neuroscience · doi:10.1037/0735-7044.116.6.1014 · Cited by 12 · see citing works
Developmental changes in pacemaker currents in mouse locus coeruleus neurons
de Oliveira, R. B., Gravina, F. S., Lim, R., Brichta, A. M., Callister, R. J., & Helden, D. F. V. (2011) · Brain Research · doi:10.1016/j.brainres.2011.09.053 · Cited by 12 · see citing works
“In rats the prevalence of spontaneously firing neurons was not reduced with development (Nakamura et al., 1987; North and Williams, 1985; Williams et al., 1984).”
A transient expression of functional α2-adrenergic receptors in white matter of the developing brain
Sanders, J. D., Happe, H. K., & Murrin, L. C. (2005) · Synapse · doi:10.1002/syn.20174 · Cited by 12 · see citing works
“example, the locus coeruleus is much more sensitive to tactile stimuli in early development than it is in the adult (Nakamura et al., 1987).”
Developmental Neurobiology of the Rat Attachment System and Its Modulation by Stress
Bisaz, R., & Sullivan, R. M. (2012) · Behavioral Sciences · doi:10.3390/bs2020079 · Cited by 11 · see citing works
“1 sec stroking or electric foot shock, the adult LC shows only a millisecond excitatory response to the same type of stimulations [100,101,110,111].”
BackgroundJacqueline, T., Sullivan, R. M., & Leon, M. (1988) · Developmental Psychobiology · doi:10.1002/dev.420210609 · Cited by 10 · see citing works
Air-stepping in neonatal rats: A comparison of L-dopa injection and olfactory stimulation.
Jamon, M., Maloum, I., Riviere, G., et al. (2002) · Behavioral Neuroscience · doi:10.1037//0735-7044.116.6.1014 · Cited by 10 · see citing works
Rančić, V., Rawal, B., Panaitescu, B., et al. (2018) · Neuroscience Letters · doi:10.1016/j.neulet.2018.02.020 · Cited by 9 · see citing works
Changes in properties of neuronal responses in two cortical taste areas in rats of various ages
Ogawa, H., Hasegawa, K., Ohgushi, M., & Murayama, N. (1994) · Neuroscience Research · doi:10.1016/0168-0102(94)90082-5 · Cited by 9 · see citing works
Ecologically relevant neurobehavioral assessment of the development of threat learningPreprint
Boulanger-Bertolus, J., Mouly, A., & Sullivan, R. M. (2016) · Learning & Memory · doi:10.1101/lm.042218.116 · Cited by 9 · see citing works
Nakamura, S., Nakayama, K., Mochizuki, A., et al. (2014) · Journal of Neurophysiology · doi:10.1152/jn.00276.2013 · Cited by 8 · see citing works
“Because the conduction velocities of axons are slow in neonatal animals (Nakamura et al. 1987; Walton and Navarrete 1991) and at low temperature and they decrease with cooling (Chatfield et al. 1948; Gasser 1931), the long antidromic latencies in this study were likely due to the immature state of…”
BackgroundSelf-citationShirokawa, T., Ishida, Y., & Isobe, K.-I. (2000) · Neuroscience Letters · doi:10.1016/s0304-3940(00)01257-x · Cited by 8 · see citing works
Ghosh, A., Mukherjee, B., Chen, X., & Yuan, Q. (2017) · Learning & Memory · doi:10.1101/lm.044818.116 · Cited by 8 · see citing works
“Early odor preference learning occurs in a sensitive post-natal period and terminates around post-natal day (PD) 10 (Sullivan et al. 2000) when a tactile stimulus no longer triggers sufficient norepinephrine release (Nakamura et al. 1987).”
Meng, Q., Garcia‐García, Á. L., Dranovsky, A., & Leonardo, E. D. (2023) · Scientific Reports · doi:10.1038/s41598-023-29175-x · Cited by 7 · see citing works
“The ability of NE to modulate brain functions develops postnatally as the maturing LC begins to exhibit activity in response to environmental changes (Nakamura et al., 1987).”
Background
- 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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