Skip to main content
Log in

Effects of negative air ions on activity of neural substrates involved in autonomic regulation in rats

  • Original Paper
  • Published:
International Journal of Biometeorology Aims and scope Submit manuscript

Abstract

The neural mechanism by which negative air ions (NAI) mediate the regulation of autonomic nervous system activity is still unknown. We examined the effects of NAI on physiological responses, such as blood pressure (BP), heart rate (HR), and heart rate variability (HRV) as well as neuronal activity, in the paraventricular nucleus of the hypothalamus (PVN), locus coeruleus (LC), nucleus ambiguus (NA), and nucleus of the solitary tract (NTS) with c-Fos immunohistochemistry in anesthetized, spontaneously breathing rats. In addition, we performed cervical vagotomy to reveal the afferent pathway involved in mediating the effects of NAI on autonomic regulation. NAI significantly decreased BP and HR, and increased HF power of the HRV spectrum. Significant decreases in c-Fos positive nuclei in the PVN and LC, and enhancement of c-Fos expression in the NA and NTS were induced by NAI. After vagotomy, these physiological and neuronal responses to NAI were not observed. These findings suggest that NAI can modulate autonomic regulation through inhibition of neuronal activity in PVN and LC as well as activation of NA neurons, and that these effects of NAI might be mediated via the vagus nerves.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Abercrombie ED, Jacobs BL (1987) Single-unit response of noradrenergic neurons in the locus coeruleus of freely moving cats. I. Acutely presented stressful and nonstressful stimuli. J Neurosci 7:2837–2843

    CAS  Google Scholar 

  • Akine A, Montanaro M, Allen AM (2003) Hypothalamic paraventricular nucleus inhibition decreases renal sympathetic nerve activity in hypertensive and normotensive rats. Auton Neurosci 108:17–21

    Article  CAS  Google Scholar 

  • Buckalew LW, Rizzuto AP (1982) Subjective response to negative air ion exposure. Aviat Space Environ Med 53:822–823

    CAS  Google Scholar 

  • Cechetto DF, Saper CB (1988) Neurochemical organization of the hypothalamic projection to the spinal cord in the rat. J Comp Neurol 272:579–604

    Article  CAS  Google Scholar 

  • Chen YY, Huang ZS (1997) Stimulation of locus coeruleus increases arterial pressure in rabbits. Zhongguo Yaoli Xuebao 18:437–440

    CAS  Google Scholar 

  • Chitravanshi VC, Agarwal SK, Calaresu FR (1991) Microinjection of glycine into the nucleus ambiguus elicits tachycardia in spinal rats. Brain Res 566:290–294

    Article  CAS  Google Scholar 

  • Ciriello J, Calaresu FR (1980) Distribution of vagal cardioinhibitory neurons in the medulla of the cat. Am J Physiol 238:R57–R64

    CAS  Google Scholar 

  • Corbett EK, Batten TF, Kaye JC, Deuchars J, McWilliam PN (1999) Labelling of rat vagal preganglionic neurones by carbocyanine dye DiI applied to the heart. Neuroreport 10:1177–1181

    Article  CAS  Google Scholar 

  • Curran T, Franza Jr. BR (1988) Fos and Jun: the AP-1 connection. Cell 55:395–397

    Article  CAS  Google Scholar 

  • Goldstein N, Arshavskaya TV (1997) Is atmospheric superoxide vitally necessary? Accelerated death of animals in a quasi-neutral electric atmosphere. Z Naturforsch 52:396–404

    CAS  Google Scholar 

  • Guevara-Aguilar R, Jimenez-Montufar LL, Garcia-Diaz DE, Wayner MJ, Armstrong DL (1988) Olfactory and visceral projections to the paraventricular nucleus. Brain Res Bull 20:799–801

    Article  CAS  Google Scholar 

  • Gurtu S, Pant KK, Sinha JN, Bhargava KP (1984) An investigation into the mechanism of cardiovascular responses elicited by electrical stimulation of locus coeruleus and subcoeruleus in the cat. Brain Res 301:59–64

    Article  CAS  Google Scholar 

  • Hawkins LH, Barker T (1978) Air ions and human performance. Ergonomics 21:273–278

    Article  CAS  Google Scholar 

  • Haxhiu MA, Loewy AD (1996) Central connections of the motor and sensory vagal systems innervating the trachea. J Auton Nerv Syst 57:49–56

    Article  CAS  Google Scholar 

  • Hayakawa T, Zheng JQ, Yajima Y (1997) Direct synaptic projections to esophageal motoneurons in the nucleus ambiguus from the nucleus of the solitary tract of the rat. J Comp Neurol 381:18–30

    Article  CAS  Google Scholar 

  • Hsieh JH, Chen RF, Wu JJ, Yen CT, Chai CY (1998) Vagal innervation of the gastrointestinal tract arises from dorsal motor nucleus while that of the heart largely from nucleus ambiguus in the cat. J Auton Nerv Syst 70:38–50

    Article  CAS  Google Scholar 

  • Iwama H (2004) Negative air ions created by water shearing improve erythrocyte deformability and aerobic metabolism. Indoor Air 14:293–297

    Article  CAS  Google Scholar 

  • Jones BE, Yang TZ (1985) The efferent projections from the reticular formation and the locus coeruleus studied by anterograde and retrograde axonal transport in the rat. J Comp Neurol 242:56–92

    Article  CAS  Google Scholar 

  • Ju K, Kubo T (1997) Power spectral analysis of autonomic nervous activity in spontaneously hypertensive rats. Biomed Sci Instrum 33:338–343

    CAS  Google Scholar 

  • Kannan H, Hayashida Y, Yamashita H (1989) Increase in sympathetic outflow by paraventricular nucleus stimulation in awake rats. Am J Physiol 256:R1325–R1330

    CAS  Google Scholar 

  • Kavet R (1987) Hypothetical neural substrates for biological responses to air ions. In: Cherry J, Kavet R (eds) Air ions: Physical and Biological Aspects, CRC, UK

  • Kita I, Seki Y, Nakatani Y, Fumoto M, Oguri M, Sato-Suzuki I, Arita H (2006) Corticotropin-releasing factor neurons in the hypothalamic paraventricular nucleus are involved in arousal/yawning response of rats. Behav Brain Res 169:48–56

    Article  CAS  Google Scholar 

  • Krueger AP, Smith RF (1958) The effects of air ions of the living mammalian trachea. J Gen Physiol 42:69–82

    Article  CAS  Google Scholar 

  • Krueger AP, Reed EJ (1976) Biological impact of small air ions. Science 193:1209–1213

    Article  CAS  Google Scholar 

  • Livanova LM, Levshina IP, Nozdracheva LV, Elbakidze MG, Airapetyants MG (1999) The protective effects of negative air ions in acute stress in rats with different typological behavioral characteristics. Neurosci Behav Physiol 29:393–395

    Article  CAS  Google Scholar 

  • Loughlin SE, Foote SL, Bloom FE (1986) Efferent projections of nucleus locus coeruleus: topographic organization of cells of origin demonstrated by three-dimensional reconstruction. Neuroscience 18:291–306

    Article  CAS  Google Scholar 

  • Malliani A, Pagani M, Lombardi F, Cerutti S (1991) Cardiovascular neural regulation explored in the frequency domain. Circulation 84:482–492

    Article  CAS  Google Scholar 

  • Miyawaki T, Kawamura H, Komatsu K, Yasugi T (1991) Chemical stimulation of the locus coeruleus: inhibitory effects on hemodynamics and renal sympathetic nerve activity. Brain Res 568:101–108

    Article  CAS  Google Scholar 

  • Neff RA, Mihalevich M, Mendelowitz D (1998) Stimulation of NTS activates NMDA and non-NMDA receptors in rat cardiac vagal neurons in the nucleus ambiguus. Brain Res 792:277–282

    Article  CAS  Google Scholar 

  • Nosaka S, Yamamoto T, Yasunaga K (1979) Localization of vagal cardioinhibitory preganglionic neurons with rat brain stem. J Comp Neurol 186:79–92

    Article  CAS  Google Scholar 

  • Pacak K, Palkovits M (2001) Stressor specificity of central neuroendocrine responses: implications for stress-related disorders. Endocr Rev 22:502–548

    Article  CAS  Google Scholar 

  • Paxinos G, Watson C (1997) The Rat Brain in stereotaxic Coordinates, (3rd edn). Academic Press, Tokyo

  • Perez-Fontan JJ, Velloff CR (2001) Labeling of vagal motoneurons and central afferents after injection of cholera toxin B into the airway lumen. Am J Physiol Lung Cell Mol Physiol 280:L152–L164

    CAS  Google Scholar 

  • Proudfit HK, Clark FM (1991) The projections of locus coeruleus neurons to the spinal cord. Prog Brain Res 88:123–141

    Article  CAS  Google Scholar 

  • Pyner S, Coote JH (2000) Identification of branching paraventricular neurons of the hypothalamus that project to the rostroventrolateral medulla and spinal cord. Neuroscience 100:549–556

    Article  CAS  Google Scholar 

  • Ricardo JA, Koh ET (1978) Anatomical evidence of direct projections from the nucleus of the solitary tract to the hypothalamus, amygdala, and other forebrain structures in the rat. Brain Res 153:1–2

    Article  CAS  Google Scholar 

  • Ross CA, Ruggiero DA, Reis DJ (1985) Projections from the nucleus tractus solitarii to the rostral ventrolateral medulla. J Comp Neurol 242:511–534

    Article  CAS  Google Scholar 

  • Ryushi T, Kita I, Sakurai T, Yasumatsu M, Isokawa M, Aihara Y, Hama K (1998) The effect of exposure to negative air ions on the recovery of physiological responses after moderate endurance exercise. Int J Biometeorol 41:132–136

    Article  CAS  Google Scholar 

  • Sawchenko PE, Swanson LW (1982) Immunohistochemical identification of neurons in the paraventricular nucleus of the hypothalamus that project to the medulla or to the spinal cord in the rat. J Comp Neurol 205:260–272

    Article  CAS  Google Scholar 

  • Shafton AD, Ryan A, Badoer E (1998) Neurons in the hypothalamic paraventricular nucleus send collaterals to spinal cord and to the rostral ventrolateral medulla in the rat. Brain Res 801:239–243

    Article  CAS  Google Scholar 

  • Sheng M, Greenberg ME (1990) The regulation and function of c-fos and other immediate early genes in the nervous system. Neuron 4:477–485

    Article  CAS  Google Scholar 

  • Sovijarvi ARA, Rosset S, Hyvarinen J, Franssila A, Graeffe G, Lehtimaki M (1979) Effect of air ionization on heart rate and perceived exertion during a bicycle exercise test. A double-blind cross-over study. Eur J Appl Physiol 41:285–291

    Article  CAS  Google Scholar 

  • Standish A, Enquist LW, Schwaber JS (1994) Innervation of the heart and its central medullary origin defined by viral tracing. Science 263:232–234

    Article  CAS  Google Scholar 

  • Stauss HM (2003) Heart rate variability. Am J Physiol Regul Integr Comp Physiol 285:R927–R931

    Article  CAS  Google Scholar 

  • Sved AF, Cano G, Passerin AM, Rabin BS (2002) The locus coeruleus, Barrington’s nucleus, and neural circuits of stress. Physiol Behav 77:737–742

    Article  CAS  Google Scholar 

  • Taylor EW, Jordan D, Coote JH (1999) Central control of the cardiovascular and respiratory systems and their interactions in vertebrates. Physiol Rev 79:855–916

    CAS  Google Scholar 

  • Tucker DC, Saper CB (1985) Specificity of spinal projections from hypothalamic and brainstem areas which innervate sympathetic preganglionic neurons. Brain Res 360:159–164

    Article  CAS  Google Scholar 

  • Van Bockstaele EJ, Peoples J, Telegan P (1999) Efferent projections of the nucleus of the solitary tract to peri-locus coeruleus dendrites in rat brain: evidence for a monosynaptic pathway. J Comp Neurol 412:410–428

    Article  Google Scholar 

  • Watanabe I, Noro H, Ohtsuka Y, Mano Y, Agishi Y (1997) Physical effects of negative air ions in a wet sauna. Int J Biometeorol 40:107–112

    Article  CAS  Google Scholar 

  • Yates A, Gray FB, Misiaszek JI, Wolman W (1986) Air ions: past problem and future directions. Environ Int 12:99–108

    Article  Google Scholar 

  • Yamada R, Yanoma S, Akaike M, Tsuburaya A, Sugimasa Y, Takemiya S, Motohashi H, Rino Y, Takanashi Y, Imada T (2006) Water-generated negative air ions activate NK cell and inhibit carcinogenesis in mice. Cancer Lett 239:190–197

    Article  CAS  Google Scholar 

  • Zahner MR, Pan HL (2005) Role of paraventricular nucleus in the cardiogenic sympathetic reflex in rats. Am J Physiol Regul Integr Comp Physiol 288:R420–R426

    Article  CAS  Google Scholar 

  • Zhang K, Li YF, Patel KP (2002) Reduced endogenous GABA-mediated inhibition in the PVN on renal nerve discharge in rats with heart failure. Am J Physiol Regul Integr Comp Physiol 282:R1006–R1015

    Article  CAS  Google Scholar 

Download references

Acknowledgment

The present study was in part supported by a grant from the Selective Research Fund of Tokyo Metropolitan University.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Ichiro Kita.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Suzuki, S., Yanagita, S., Amemiya, S. et al. Effects of negative air ions on activity of neural substrates involved in autonomic regulation in rats. Int J Biometeorol 52, 481–489 (2008). https://doi.org/10.1007/s00484-007-0143-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00484-007-0143-2

Keywords

Navigation