Effects of inflammation on hippocampus and substantia nigra responses to novelty in healthy human participants

Neuropsychopharmacology

Volumn 40, Issue 4, 2015, Pages 831-838

  Harrison, Neil A ^a,b   Cercignani, Mara ^a   Voon, Valerie ^c   Critchley, Hugo D ^a,b  

^a BRIGHTON AND SUSSEX MEDICAL SCHOOL   (United Kingdom)

^b UNIVERSITY OF SUSSEX   (United Kingdom)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 1 RECEPTOR BLOCKING AGENT; INTERLEUKIN 6; PLACEBO; TUMOR NECROSIS FACTOR ALPHA; TYPHOID VACCINE; BACTERIAL POLYSACCHARIDE; CYTOKINE; OXYGEN; TYPHOID PARATYPHOID VACCINE; VI POLYSACCHARIDE VACCINE, TYPHOID;

ADULT; ANGULAR GYRUS; ARTICLE; CONTROLLED STUDY; CROSSOVER PROCEDURE; CYTOKINE RESPONSE; DOPAMINERGIC NERVE CELL; DOUBLE BLIND PROCEDURE; ENCEPHALITIS; EXPERIMENTAL INFLAMMATION; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HIPPOCAMPUS; HUMAN; HUMAN EXPERIMENT; ILLNESS BEHAVIOR; INFERIOR TEMPORAL GYRUS; MALE; MIDDLE FRONTAL GYRUS; NORMAL HUMAN; PRIMARY IMMUNE RESPONSE; PRIORITY JOURNAL; RANDOMIZED CONTROLLED TRIAL; SALMONELLA ENTERICA SEROVAR TYPHI; SUBSTANTIA NIGRA; TYPHOID FEVER; VACCINATION; BLOOD; BRAIN MAPPING; EXPLORATORY BEHAVIOR; INFLAMMATION; METABOLISM; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOLOGY; PHOTOSTIMULATION; PHYSIOLOGY; PSYCHOPHYSICS; VASCULARIZATION; YOUNG ADULT;

ADULT; BRAIN MAPPING; CROSS-OVER STUDIES; CYTOKINES; DOUBLE-BLIND METHOD; EXPLORATORY BEHAVIOR; FEMALE; HEALTHY VOLUNTEERS; HIPPOCAMPUS; HUMANS; INFLAMMATION; MAGNETIC RESONANCE IMAGING; MALE; OXYGEN; PHOTIC STIMULATION; POLYSACCHARIDES, BACTERIAL; PSYCHOPHYSICS; SUBSTANTIA NIGRA; TYPHOID-PARATYPHOID VACCINES; YOUNG ADULT;

EID: 84925157112     PISSN: 0893133X     EISSN: 1740634X     Source Type: Journal    
DOI: 10.1038/npp.2014.222     Document Type: Article

References (48)

1. Barrientos RM, Higgins EA, Sprunger DB, Watkins LR, Rudy JW, Maier SF (2002). Memory for context is impaired by a post context exposure injection of interleukin-1 beta into dorsal hippocampus. Behav Brain Res 134: 291-298.
2. Bellinger FP, Madamba S, Siggins GR (1993). Interleukin 1 beta inhibits synaptic strength and long-term potentiation in the rat CA1 hippocampus. Brain Res 628: 227-234.
3. Berlyne DE (1955). The arousal and satiation of perceptual curiosity in the rat. J Comp Physiol Psychol 48: 238-246.
4. Berridge KC (2007). The debate over dopamine's role in reward: the case for incentive salience. Psychopharmacology 191: 391-431.
5. Bluthe RM, Crestani F, Kelley KW, Dantzer R (1992). Mechanisms of the behavioral effects of interleukin-1: role of prostaglandins and CRF. Ann N Y Acad Sci 650: 268-275.
6. Brydon L, Edwards S, Mohamed-Ali V, Steptoe A (2004). Socioeconomic status and stress-induced increases in interleukin-6. Brain Behav Immun 18: 281-290.
7. Brydon L, Harrison NA, Walker C, Steptoe A, Critchley HD (2008). Peripheral inflammation is associated with altered substantia nigra activity and psychomotor slowing in humans. Biol Psychiatry 63: 1022-1029.
8. Bunzeck N, Duzel E (2006). Absolute coding of stimulus novelty in the human substantia nigra/VTA. Neuron 51: 369-379.
9. Deichmann R, Gottfried JA, Hutton C, Turner R (2003). Optimized EPI for fMRI studies of the orbitofrontal cortex. Neuroimage 19: 430-441.
10. Dunn AJ, Antoon M, Chapman Y (1991). Reduction of exploratory behavior by intraperitoneal injection of interleukin-1 involves brain corticotropin-releasing factor. Brain Res Bull 26: 539-542.
11. Duzel E, Bunzeck N, Guitart-Masip M, Duzel S (2010). Noveltyrelated Motivation of Anticipation and exploration by Dopamine (NOMAD): Implications for healthy ageing. Neurosci Biobehav Rev 34: 660-669.
12. Flicker C, Geyer MA (1982). Behavior during hippocampal microinfusions. I. Norepinephrine and diversive exploration. Brain Res Rev 4: 79-103.
13. Gibertini M (1996). IL1 beta impairs relational but not procedural rodent learning in a water maze task. Adv Exp Med Biol 402: 207-217.
14. Haba R, Shintani N, Onaka Y, Wang H, Takenaga R, Hayata A et al (2012). Lipopolysaccharide affects exploratory behaviors towards novel objects by impairing cognition and /or motivation in mice: possible role of activation of the central amygdala. Behav Brain Res 228: 423-431.
15. Harrison NA, Brydon L, Walker C, Gray MA, Steptoe A, Dolan RJ et al (2009). Neural origins of human sickness in interoceptive responses to inflammation. Biol Psychiatry 66: 415-422.
16. Harrison NA, Doeller CF, Voon V, Burgess N, Critchley HD (2014). Peripheral inflammation acutely impairs human spatial memory via actions on medial temporal lobe glucose metabolism. Biol Psychiatry 76: 585-593.
17. Hart BL (1988). Biological basis of the behavior of sick animals. Neurosci Biobehav Rev 12: 123-137.
18. Horvitz JC, Stewart T, Jacobs BL (1997). Burst activity of ventral tegmental dopamine neurons is elicited by sensory stimuli in the awake cat. Brain Res 759: 251-258.
19. Howard LR, Kumaran D, O lafsdóttir HF, Spiers HF (2011). Double dissociation between hippocampal and parahippocampal responses to object-background context and scene novelty. J Neurosci 31: 5253-5261.
20. Hyman SE, Malenka RC, Nestler EJ (2006). Neural mechanisms of addiction: the role of reward-related learning and memory. Annu Rev Neurosci 29: 565-598.
21. Jenkins TA, Amin E, Pearce JM, Brown MW, Aggleton JP (2004). Novel spatial arrangements of familiar visual stimuli promote activity in the rat hippocampal formation but not the parahippocampal cortices: a c-fos expression study. Neuroscience 124: 43-52.
22. Kakade S, Dayan P (2002). Dopamine: generalization and bonuses. Neural Netw 15: 549-559.
23. Katsuki H, Nakai S, Hirai Y, Akaji K, Kiso Y, Satoh M (1990). Interleukin-1b inhibits long-term potentiation in the CA3 region of mouse hippocampal slices. Eur J Pharmacol 181: 323-332.
24. Kawashima N, Kusnecov AW (2002). Effects of staphylococcal enterotoxin A on pituitary-adrenal activation and neophobic behavior in the C57BL/6 mouse. J Neuroimmunol 123: 41-49.
25. Knight RT (1996). Contribution of human hippocampal region to novelty detection. Nature 383: 256-259.
26. Knutson B, Cooper JC (2006). The lure of the unknown. Neuron 51: 280-282.
27. Kusnecov AW, Liang R, Shurin G (1999). T-lymphocyte activation increases hypothalamic and amygdaloid expression of CRH mRNA and emotional reactivity to novelty. J Neurosci 19: 4533-4543.
28. Legault M, Wise RA (2001). Novelty-evoked elevations of nucleus accumbens dopamine: dependence on impulse flow from the ventral subiculum and glutamatergic neurotransmission in the ventral tegmental area. Eur J Neurosci 13: 819-828.
29. Lima SL, Dill LM (1990). Behavioral decisions made under the risk of predation: a review and prospectus. Can J Zool 68: 619-640.
30. Lisman JE, Grace AA (2005). The hippocampal-VTA loop: controlling the entry of information into long-term memory. Neuron 46: 703-713.
31. Niv Y, Daw ND, Joel D, Dayan P (2007). Tonic dopamine: opportunity costs and the control of response vigor. Psychopharmacology 191: 507-520.
32. Pacheco-López G, Bermúdez-Rattoni F (2011). Brain-immune interactions and the neural basis of disease-avoidant ingestive behavior. Phil Trans R Soc B 366: 3389-3405.
33. Panksepp J (1998). Affective Neuroscience: The Foundations of Human and Animal Emotions. 1st edn. Oxford University Press: New York, NY, USA.
34. Perry VH, Cunningham C, Holmes C (2007). Systemic infections and inflammation affect chronic neurodegeneration. Nat Rev Immunol 7: 161-167.
35. Pessiglione M, Seymour B, Flandin G, Dolan RJ, Frith CD (2006). Dopamine-dependent prediction errors underpin reward-seeking behavior in humans. Nature 442: 1042-1045.
36. Ranganath C, Rainer G (2003). Neural mechanisms for detecting and remembering novel events. Nature Rev Neurosci 4: 193-202.
37. Robbins TW, Everitt BJ (2007). A role for mesencephalic dopamine in activation: commentary on Berridge (2006). Psychopharmacology 191: 433-437.
38. Sanderson DJ, Cunningham C, Deacon RM, Bannerman DM, Perry VH, Rawlins JN (2009). A double dissociation between the effects of sub-pyrogenic systemic inflammation and hippocampal lesions on learning. Behav Brain Res 201: 103-111.
39. Schaller M, Park JH (2011). The behavioral immune system (and why it matters). Curr Dir Psychol Sci 20: 99-103.
40. Schultz W (1998). Predictive reward signal of dopamine neurons. J Neurophys 80: 1-27.
41. Slotnick SD, Moo LR, Segal JB, Hart J (2003). Distinct prefrontal cortex activity associated with item memory and source memory for visual shapes. Cogn Brain Res 17: 75-82.
42. Spadaro F, Dunn AJ (1990). Intracerebroventricular administration of interleukin-1 to mice alters investigation of stimuli in a novel environment. Brain Behav Immun 4: 308-322.
43. Stern CE, Corkin S, Gonzalez RG, Guimaraes AR, Baker JR, Jennings PJ et al (1996). The hippocampal formation participates in novel picture encoding: Evidence from functional magnetic resonance imaging. Proc Natl Acad Sci USA 93: 8660-8665.
44. Straub RH, Cutolo M, Buttgereit F, Pongratz G (2010). Energy regulation and neuroendocrine-immune control in chronic inflammatory diseases. J Intern Med 267: 543-560.
45. Vinogradova OS (2001). Hippocampus as comparator: role of the two input and two output systems of the hippocampus in selection and registration of information. Hippocampus 11: 578-598.
46. Wittmann BC, Daw ND, Seymour B, Dolan RJ (2008). Striatal activity underlies novelty-based choice in humans. Neuron 58: 967-973.
47. Yang CR, Mogenson GJ (1987). Hippocampal signal transmission to the pedunculopontine nucleus and its regulation by dopamine D2 receptors in the nucleus accumbens: An electrophysiological and behavioral study. Neuroscience 23: 1041-1055.
48. Yirmiya R, Goshen I (2011). Immune modulation of learning, memory, neural plasticity and neurogenesis. Brain Behav Immun 25: 181-213.