Interleukin‐1β modulates state‐dependent discharge activity of preoptic area and basal forebrain neurons: role in sleep regulation
Open accessAbstract
Interleukin‐1β (IL‐1) is a pro‐inflammatory cytokine that has been implicated in the regulation of nonrapid eye movement (nonREM) sleep. IL‐1, IL‐1 receptors and the IL‐1 receptor antagonist (ra) are present normally in discrete brain regions, including the preoptic area (POA) of the hypothalamus and the adjoining magnocellular basal forebrain (BF). The POA/BF have been implicated in the regulation of sleep–wakefulness. We hypothesized that IL‐1 promotes nonREM sleep, in part by altering the state‐dependent discharge activity of POA/BF neurons. We recorded the sleep–wake discharge profiles of 83 neurons in the lateral POA/BF and assessed the effects of IL‐1, IL‐1ra, and IL‐ra + IL‐1 delivered through a microdialysis probe on state‐dependent neuronal discharge activity. IL‐1 decreased the discharge rate of POA/BF neurons as a group (n = 55) but wake‐related and sleep‐related neurons responded differently. IL‐1 significantly decreased the discharge rate of wake‐related neurons. Of 24 wake‐related neurons studied, 19 (79%) neurons exhibited a greater than 20% change in their discharge in the presence of IL‐1 during waking. IL‐1 suppressed the discharge activity of 18 of 19 responsive neurons. Of 13 sleep‐related neurons studied, IL‐1 increased the discharge activity of five and suppressed the discharge activity of four neurons. IL‐1ra increased the discharge activity of four of nine neurons and significantly attenuated IL‐1‐induced effects on neuronal activity of POA/BF neurons (n = 19). These results suggest that the sleep‐promoting effects of IL‐1 may be mediated, in part, via the suppression of wake‐related neurons and the activation of a subpopulation of sleep‐related neurons in the POA/BF.
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Proinflammatory cytokines can stimulate (a subset of) sleep-promoting neurons in the preoptic area and basal forebrain.
“Indeed, proinflammatory cytokines can actively inhibit wake-promoting neurons and stimulate (a subset of) sleep-promoting neurons in the preoptic area and basal forebrain (Alam et al., 2004).”
From The role of inflammation in core features of depression: Insights from paradigms using exogenously-induced inflammation. (2018) · cites this paper as Alam et al., 2004
Proinflammatory cytokines can actively inhibit wake-promoting neurons.
“Indeed, proinflammatory cytokines can actively inhibit wake-promoting neurons and stimulate (a subset of) sleep-promoting neurons in the preoptic area and basal forebrain (Alam et al., 2004).”
From The role of inflammation in core features of depression: Insights from paradigms using exogenously-induced inflammation. (2018) · cites this paper as Alam et al., 2004
Within the hypothalamus, IL-1 increases c-Fos and inhibits wake-active neurons.
“Within the hypothalamus, IL-1 increases c-Fos (Baker et al, 2005) and inhibits wake-active neurons (Alam et al, 2004).”
From Sleep health: Reciprocal regulation of sleep and innate immunity (2017) · cites this paper as Alam et al, 2004
IL-1beta, TNFalpha, and IL-18 are inducers of nonrapid eye movement sleep.
“IL-1b,21 TNFa22, and IL-1823 are inducers of nonrapid eye movement (nREM) sleep.”
From The Gut Microbiome and the Brain (2014) · cites this paper as [21]
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Self-citation
- Authors
- Alam, M. N., McGinty, D., Bashir, T., Kumar, S., Imeri, L., Opp, M. R., & Szymusiak, R.
- Affiliations
- VA Greater Los Angeles Healthcare System (US)
- University of California, Los Angeles (US)
- University of Milan (IT)
- University of Michigan (US)
- Corresponding author
- Szymusiak, Ronald
- Venue
- European Journal of Neuroscience
- Publisher
- Wiley
- Published
- 2004-06-21
- Volume
- 20
- Issue
- 1
- Pages
- 207-216
- ISSN
- 0953-816X (ISSN-L)
- 1460-9568
- OpenAlex
- W2126867943
- Cited by
- 108
- References
- 63
- Citations by year
- 2026: 3 · 2025: 6 · 2024: 6 · 2023: 3 · 2022: 6 · 2021: 2 · 2020: 7 · 2019: 5 · 2018: 2 · 2017: 1 · 2016: 6 · 2015: 4 · 2014: 4 · 2013: 7 · 2012: 7
- FWCI
- 3.53
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- European Journal of Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- Deep Blue (University of Michigan) (submittedVersion)
- Funders
- National Institutes of Health (5p50hl060296-10, 1r01mh061354-01)
- National Heart, Lung, and Blood Institute (HL 60296)
- National Institute of Mental Health (MH-63323, R01MH047480, MH47480, MH-64843, R01MH063323, MH61354)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Sleep and Wakefulness Research
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Neuroscience of respiration and sleep
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Circadian rhythm and melatonin
- Keywords
- IL-1β, interleukin-1 receptor antagonist, sleep regulation, preoptic area, basal forebrain, sleep-wake states, cytokines, hypothalamus, microdialysis
- MeSH terms
- Action Potentials, Animals, Electroencephalography, Interleukin-1, Male, Neurons, Preoptic Area, Sialoglycoproteins, Sleep, Wakefulness, Prosencephalon, Rats, Sprague-Dawley, Polysomnography, Rats, Interleukin 1 Receptor Antagonist Protein
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