Peripheral inflammation is associated with altered substantia nigra activity and psychomotor slowing in humans
Open accessAbstract
BackgroundSystemic infections commonly cause sickness symptoms including psychomotor retardation. Inflammatory cytokines released during the innate immune response are implicated in the communication of peripheral inflammatory signals to the brain.MethodsWe used functional magnetic resonance brain imaging (fMRI) to investigate neural effects of peripheral inflammation following typhoid vaccination in 16 healthy men, using a double-blind, randomized, crossover-controlled design.ResultsVaccination had no global effect on neurovascular coupling but markedly perturbed neural reactivity within substantia nigra during low-level visual stimulation. During a cognitive task, individuals in whom typhoid vaccination engendered higher levels of circulating interleukin-6 had significantly slower reaction time responses. Prolonged reaction times and larger interleukin-6 responses were associated with evoked neural activity within substantia nigra.ConclusionsOur findings provide mechanistic insights into the interaction between inflammation and neurocognitive performance, specifically implicating circulating cytokines and midbrain dopaminergic nuclei in mediating the psychomotor consequences of systemic infection. Systemic infections commonly cause sickness symptoms including psychomotor retardation. Inflammatory cytokines released during the innate immune response are implicated in the communication of peripheral inflammatory signals to the brain. We used functional magnetic resonance brain imaging (fMRI) to investigate neural effects of peripheral inflammation following typhoid vaccination in 16 healthy men, using a double-blind, randomized, crossover-controlled design. Vaccination had no global effect on neurovascular coupling but markedly perturbed neural reactivity within substantia nigra during low-level visual stimulation. During a cognitive task, individuals in whom typhoid vaccination engendered higher levels of circulating interleukin-6 had significantly slower reaction time responses. Prolonged reaction times and larger interleukin-6 responses were associated with evoked neural activity within substantia nigra. Our findings provide mechanistic insights into the interaction between inflammation and neurocognitive performance, specifically implicating circulating cytokines and midbrain dopaminergic nuclei in mediating the psychomotor consequences of systemic infection.
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Typhoid vaccination is associated with altered neural activity in the substantia nigra, a part of the basal ganglia involved in motor planning and reward seeking.
“typhoid vaccination has been associated with altered neural activity in the substantia nigra, a part of the basal ganglia that is involved in motor planning and reward seeking”
From From stress to inflammation and major depressive disorder: A social signal transduction theory of depression. (2014) · cites this paper as Brydon, Harrison, Walker, Steptoe, & Critchley, 2008
After typhoid vaccination, individuals with higher vaccine-induced IL-6 levels had significantly slower reaction times on both incongruent and congruent Stroop trials.
“Brydon et al. (2008) examined Stroop performance after typhoid vaccination, and found that individuals with higher vaccine-induced IL-6 levels had significantly slower reaction times across both incongruent and congruent trials.”
From The role of inflammation in core features of depression: Insights from paradigms using exogenously-induced inflammation. (2018) · cites this paper as Brydon et al., 2008
Inflammation did not impair inhibitory control but instead led to overall psychomotor slowing and/or decreased motivation.
“Thus, inflammation did not impair inhibitory control, but rather led to an overall psychomotor slowing and/or decrease in motivation (Brydon et al., 2008).”
From The role of inflammation in core features of depression: Insights from paradigms using exogenously-induced inflammation. (2018) · cites this paper as Brydon et al., 2008
Exogenous stimulation of proinflammatory cytokines leads to reports of increased fatigue across endotoxin, typhoid vaccination, and IFN-α paradigms.
“Studies across the endotoxin, typhoid vaccination, and IFN-α paradigms have consistently shown that exogenous stimulation of proinflammatory cytokines leads to reports of increased fatigue (Brydon et al., 2008; Capuron et al., 2002; Dowell et al., 2016; Eisenberger et al., 2010a; Grigoleit et al., 2011; Harrison et al., 2009; Moieni et al., 2015) and decreases in ratings of vigor (Dowell et al., 2”
From The role of inflammation in core features of depression: Insights from paradigms using exogenously-induced inflammation. (2018) · cites this paper as Brydon et al., 2008
Greater IL-6 following typhoid vaccination was associated with slower response times on all trials of a color-word Stroop task (both congruent and incongruent).
“Further, greater IL-6 following typhoid vaccination was associated with slower response times on all trials of a color-word Stroop task (both congruent and incongruent trials) (Brydon et al., 2008).”
From The role of inflammation in core features of depression: Insights from paradigms using exogenously-induced inflammation. (2018) · cites this paper as Brydon et al., 2008
Increases in IL-6 and decreases in motor speed were both associated with altered activation patterns (enhanced activation) in the substantia nigra.
“Notably, increases in IL-6 and decreases in motor speed were both associated with altered activation patterns (enhanced activation) in the substantia nigra (Brydon et al., 2008).”
From The role of inflammation in core features of depression: Insights from paradigms using exogenously-induced inflammation. (2018) · cites this paper as Brydon et al., 2008
Typhoid vaccine studies show increases in fatigue within 2-3 hours despite only mild, acute increases in inflammation.
“This is exemplified by typhoid vaccine studies which can lead to increases in fatigue within 2–3 hours despite eliciting only mild, acute increases in inflammation (Brydon et al., 2008).”
From The role of inflammation in core features of depression: Insights from paradigms using exogenously-induced inflammation. (2018) · cites this paper as Brydon et al., 2008
Even brief, modest rises in inflammation can produce somatic symptoms, especially fatigue.
“Mild, short-term increases in inflammation are sufficient to cause somatic symptoms, particularly fatigue.”
From The role of inflammation in core features of depression: Insights from paradigms using exogenously-induced inflammation. (2018) · cites this paper as Brydon et al., 2008
Depression and fatigue are the main side effects of treatment with interferon-alpha.
“depression and fatigue are the main side effects of treatment with IFN-α (111, 112).”
From Cytokine Research in Depression: Principles, Challenges, and Open Questions (2019) · cites this paper as [111]
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BackgroundDopamine, Immunity, and Disease
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BackgroundImmune aging, dysmetabolism, and inflammation in neurological diseases
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“Accordingly, cytokines can influence cognitive processes, including reaction time and working memory (29), that can be impaired in ADHD.”
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“In adults, IL-6 partially mediated relationships between childhood abuse and lower amygdala-vmPFC rsFC (105), and an inflammatory cytokine composite related to low salience, default mode network (DMN), and central executive inter-network rsFC in association with sub-clinical PTSD symptoms in stress-exposed firefighter…”
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“In addition, typhoid vaccination has been shown to alter activity in the substantia nigra in relation to psychomotor slowing (Brydon et al, 2008).”
BackgroundAntidepressant therapies inhibit inflammation and microglial M1-polarization
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“…2012), neural activity in ventral striatal regions is altered following administration of several inflammatory stimuli including IFN-α, typhoid vaccination, and endotoxin in psychiatrically healthy individuals (Brydon et al, 2008; Capuron et al, 2012; Eisenberger et al, 2010; Harrison et al, 2015).”
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“Similarly, lipopolysaccharide (LPS) and typhoid vaccination have been shown to have effects on basal ganglia activity (Brydon et al. 2008; Eisenberger et al. 2010), including decreased ventral striatal activation to a reward task (Eisenberger et al. 2010), suggesting that the effects on basal…”
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“In addition to these correlative data, both immediate and longterm administration of proinflammatory cytokines (or substances that induce these cytokines) cause behavioral symptoms that overlap with those found in MDD and respond to standard antidepressant therapy.(86-91) Consistent with evidence that proinflammatory…”
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“In humans, systemic inflammation through typhoid vaccination causes higher levels of circulating IL-6 levels that are associated with prolonged reaction times and increased evoked neural activity within substantia nigra (Brydon et al., 2008).”
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“The reduction in mood is correlated with plasma IL-6 levels (Brydon et al., 2008; Eisenberger et al., 2009) as is fatigue (Brydon et al.”
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Mood Disorders and Obesity: Understanding Inflammation as a Pathophysiological Nexus
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“For example, healthy males subjected to a typhoid vaccination show markedly abnormal neural reactivity within the sub- stantia nigra which was associated with psychomotor slowing (Brydon et al. 2008).”
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“kines) has been demonstrated to produce similar responses in the basal ganglia, indicating that administration of IFNα and other inflammatory inputs yield similar effects [277, 278].”
BackgroundNeuropsychiatric Comorbidity in Obesity: Role of Inflammatory Processes
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“In addition, healthy volunteers exposed to typhoid vaccination (compared with placebo) showed altered activation in the substantia nigra that was associated with reduced psychomotor speed and increased peripheral blood interleukin-6 (Brydon et al, 2008).”
BackgroundTherapeutic Implications of Brain–Immune Interactions: Treatment in Translation
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“Similarly, healthy individuals given typhoid vaccination showed increased activity in the basal ganglia using fMRI, which was associated with both increases in peripheral blood IL-6 and psychomotor slowing (Brydon et al., 2008).”
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“Similarly, immuno-activation in animals and healthy volunteers leads to fatigue, psychomotor retardation and anhedonia, which are typical somatic symptoms according to ICD-10 diagnostic criteria for depressive episode (Brydon et al., 2008; Capuron et al., 2012; Eisenberger et al., 2010; Harrison et al., 2009, 2015).”
Ghrelin's Roles in Stress, Mood, and Anxiety Regulation
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“The Salmonella typhi vaccine experimental model of inflammation induces a low-grade inflammatory response associated with an approximately threefold increase in peripheral IL-6 levels peaking 3–4 hours after vaccination (16).”
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“Increases in IL6 after typhoid vaccination have also been correlated with slowed reaction times (Brydon et al., 2008), suggesting that cytokine-induced changes in the basal ganglia can contribute to both motivational deficits and psychomotor retardation.”
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“We also previously reported psychomotor slowing after typhoid vaccination (53).”
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“30 Provoking an acute inflammatory response in healthy humans, for example via injection of endotoxin, 6,7 IL-6, 36 or IFN-b , 37 also produces symptoms similar to those seen in depression (such as fatigue, lack of motivation, anorexia, poor sleep).”
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“Other regions include the nucleus accumbens and putamen in interferon-a–induced fatigue (15), the substantia nigra in typhoid-vaccine–induced cognitive impairment (16), and the ventral striatum in response to monetary reward cues when subjects received endotoxin (17).”
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“It will thus be important for future studies to examine the effects of inflammatory challenges that do not influence cortisol (e.g., typhoid vaccination; Brydon et al., 2008).”
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- Authors
- Brydon, L., Harrison, N. A., Walker, C., Steptoe, A., & Critchley, H. D.
- Affiliations
- UCL Queen Square Institute of Neurology (GB)
- Wellcome Centre for Human Neuroimaging (GB)
- Brighton and Sussex Medical School (GB)
- Corresponding author
- Brydon, Lena
- Venue
- Biological Psychiatry
- Publisher
- Elsevier BV
- Published
- 2008-06
- Volume
- 63
- Issue
- 11
- Pages
- 1022-1029
- ISSN
- 0006-3223 (ISSN-L)
- PMC
- PMC2885493
- OpenAlex
- W2059416963
- Cited by
- 381
- References
- 48
- Citations by year
- 2026: 5 · 2025: 20 · 2024: 23 · 2023: 22 · 2022: 16 · 2021: 41 · 2020: 25 · 2019: 20 · 2018: 26 · 2017: 15 · 2016: 35 · 2015: 26 · 2014: 17 · 2013: 19 · 2012: 25
- FWCI
- 5.12
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Biological Psychiatry (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Sussex Research Online (University of Sussex) (submittedVersion)
- UCL Discovery (University College London) (submittedVersion)
- Figshare (submittedVersion, cc-by)
- ORCA Online Research @Cardiff (Cardiff University) (submittedVersion)
- Funders
- Wellcome Trust
- British Heart Foundation
- Topics
- Life Sciences › Neuroscience › Biological Psychiatry › Tryptophan and brain disorders
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Keywords
- peripheral inflammation, substantia nigra, psychomotor retardation, typhoid vaccination, interleukin-6, sickness behavior, neuroinflammation, dopaminergic midbrain, reaction time, neurovascular coupling, systemic infection, cytokines
- MeSH terms
- Adolescent, Adult, Brain Mapping, Double-Blind Method, Humans, Image Processing, Computer-Assisted, Inflammation, Magnetic Resonance Imaging, Male, Neuropsychological Tests, Oxygen, Photic Stimulation, Psychomotor Performance, Reaction Time, Substantia Nigra, Typhoid Fever, Vaccination, Interleukin-6, Cross-Over Studies, Motor Skills Disorders
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