Experimental carotid baroreceptor stimulation reduces blood flow velocities in the anterior and middle cerebral arteries of healthy individuals

  1. Reyes del Paso, Gustavo A. 1
  2. Montoro, Casandra I. 1
  3. Jennings, J. Richard 2
  4. Duschek, Stefan 3
  1. 1 Department of Psychology, University of Jaén
  2. 2 Department of Psychiatry, School of Medicine, University of Pittsburgh, Pittsburgh, USA
  3. 3 UMIT TIROL - University for Health Sciences and Technology, Hall in Tirol, Austria
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Revista:
The Journal of Physiological Sciences

ISSN: 1880-6562

Año de publicación: 2023

Volumen: 73

Número: 1

Tipo: Artículo

DOI: 10.1186/S12576-023-00871-7 GOOGLE SCHOLAR lock_openAcceso abierto editor

Otras publicaciones en: The Journal of Physiological Sciences

Resumen

This study investigated effects of experimental baroreceptor stimulation on bilateral blood flow velocities in the anterior and middle cerebral arteries (ACA and MCA) using functional transcranial Doppler sonography. Carotid baroreceptors were stimulated by neck suction in 33 healthy participants. Therefore, negative pressure (− 50 mmHg) was applied; neck pressure (+ 10 mmHg) was used as a control condition. Heart rate (HR) and blood pressure (BP) were also continuously recorded. Neck suction led to reductions in bilateral ACA and MCA blood flow velocities, which accompanied the expected HR and BP decreases; HR and BP decreases correlated positively with the ACA flow velocity decline. The observations suggest reduction of blood flow in the perfusion territories of the ACA and MCA during baroreceptor stimulation. Baroreceptor-related HR and BP decreases may contribute to the cerebral blood flow decline. The findings underline the interaction between peripheral and cerebral hemodynamic regulation in autoregulatory control of cerebral perfusion.

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Referencias bibliográficas

  • Aaslid R, Markwalder TM, Nornes H (1982) Noninvasive transcranial Doppler ultrasound recording of flow velocity in basal cerebral arteries. J Neurosurg 57:769–774. https://doi.org/10.3171/jns.1982.57.6.0769
  • Bäcker M, Knecht S, Deppe M, Lohmann H, Ringelstein EB, Henningsen H (1999) Cortical tuning: a function of anticipated stimulus intensity. NeuroReport 10:293–296. https://doi.org/10.1097/00001756-199902050-00016
  • Claydon VE, Hainsworth R (2003) Cerebral autoregulation during orthostatic stress in healthy controls and in patients with posturally related syncope. Clin Auton Res 13:321–329. https://doi.org/10.1007/s10286-003-0120-8
  • Craig AD (2002) How do you feel? Interoception: the sense of the physiological condition of the body. Nat Rev Neurosci 3:655–666. https://doi.org/10.1038/nrn894
  • Craig AD (2003) Interoception: the sense of the physiological condition of the body. Curr Opin Neurobiol 13:500–505. https://doi.org/10.1038/nrn894
  • Craig AD (2005) Forebrain emotional asymmetry: a neuroanatomical basis? Trends Cogn Sci 19:566–571. https://doi.org/10.1016/j.tics.2005.10.005
  • Critchley HD, Harrison NA (2013) Visceral influences on brain and behavior. Neuron 77:624–638. https://doi.org/10.1016/j.neuron.2013.02.008
  • Dampney RA, Polson JW, Potts PD, Hirooka Y, Horiuchi J (2003) Functional organization of brain pathways subserving the baroreceptor reflex: studies in conscious animals using immediate early gene expression. Cell Mol Neurobiol 23:597–616. https://doi.org/10.1023/A:1025080314925
  • Droste C, Kardos A, Brody S, Greenlee MW, Roskamm H, Rau H (1994) Baroreceptor stimulation: pain perception and sensory thresholds. Biol Psychol 37:101–113. https://doi.org/10.1016/0301-0511(94)90025-6
  • Duschek S, Schandry R (2003) Functional transcranial Doppler sonography as a tool in psychophysiological research. Psychophysiology 40:436–454. https://doi.org/10.1111/1469-8986.00046
  • Duschek S, Schandry R (2004) Cognitive performance and cerebral blood flow in essential hypotension. Psychophysiology 41:905–913. https://doi.org/10.1111/j.1469-8986.2004.00249.x
  • Duschek S, Hadjamu M, Schandry R (2007) Enhancement of cerebral blood flow and cognitive performance due to pharmacological blood pressure elevation in chronic hypotension. Psychophysiology 44:145–153. https://doi.org/10.1111/j.1469-8986.2006.00472.x
  • Duschek S, Heiss H, Schmidt FH, Werner N, Schuepbach D (2010) Interactions between systemic hemodynamics and cerebral blood flow during attentional processing. Psychophysiology 47:1159–1166. https://doi.org/10.1111/j.1469-8986.2010.01020.x
  • Duschek S, Werner N, Kapan N, Reyes del Paso GA (2008) Patterns of cerebral blood flow and systemic hemodynamics during arithmetic processing. J Psychophysiol 22:81–90. https://doi.org/10.1027/0269-8803.22.2.81
  • Duschek S, Werner NS, Reyes del Paso GA (2013) The behavioral impact of baroreflex function: a review. Psychophysiology 50:1183–1193. https://doi.org/10.1111/psyp.12136
  • Duschek S, Wörsching J, Reyes del Paso GA (2013) Interactions between autonomic cardiovascular regulation and cortical activity: a CNV study. Psychophysiology 50:388–397. https://doi.org/10.1111/psyp.12026
  • Duschek S, Hoffmann A, Bair A, Reyes del Paso GA, Montoro CI (2018) Cerebral blood flow modulations during proactive control in chronic hypotension. Brain Cogn 125:135–141. https://doi.org/10.1016/j.bandc.2018.06.008
  • Duschek S, Hoffmann A, Montoro CI, Bair A, Reyes del Paso GA, Ettinger U (2019) Cerebral blood flow modulations during antisaccade preparation in chronic hypotension. Psychophysiology 56(3):e13305. https://doi.org/10.1111/psyp.13305
  • Dworkin BR, Elbert T, Rau H, Birbaumer N, Pauli P, Droste C, Brunia CH (1994) Central effects of baroreceptor activation in humans: attenuation of skeletal reflexes and pain perception. Proc Natl Acad Sci USA 91:6329–6333. https://doi.org/10.1073/pnas.91.14.6329
  • Edwards L, McIntyre D, Carroll D, Ring C, France CR, Martin U (2003) Effects of artificial and natural baroreceptor stimulation on nociceptive responding and pain. Psychophysiology 40:762–769. https://doi.org/10.1111/1469-8986.00076
  • Elbert T, Rockstroh B, Lutzenberger W, Kessler M, Pietrowsky R, Birbaumer N (1988) Baroreceptor stimulation alters pain sensation depending on tonic blood pressure. Psychophysiology 25:25–29. https://doi.org/10.1111/j.1469-8986.1988.tb00953.x
  • Folino, (2007) Cerebral autoregulation and syncope. Prog Cardiovasc Dis 50:49–80. https://doi.org/10.1016/j.pcad.2007.01.001
  • Golding EM, Marrelli SP, You J, Bryan RM (2002) Endothelium-derived hyperpolarizing factor in the brain: a new regulator of cerebral blood flow? Stroke 33(3):661–663. https://doi.org/10.1161/str.33.3.661
  • Haines DE (2007) Neuroanatomy. An Atlas of Structures, Sections, and Systems. Lippincott Williams and Wilkins, Philadelphia.
  • Harder DR, Zhang C, Gebremedhin D (2002) Astrocytes function in matching blood flow to metabolic activity. News Physiol Sci 17:27–31. https://doi.org/10.1152/physiologyonline.2002.17.1.27
  • Iadecola C (2004) Neurovascular regulation in the normal brain and in Alzheimer’s disease. Nat Rev Neurosci 5:347–360. https://doi.org/10.1038/nrn1387
  • Iadecola (2017) The neurovascular unit coming of age: a journey through neurovascular coupling in health and disease. Neuron 96(1):17–42. https://doi.org/10.1016/j.neuron.2017.07.030
  • Jennings JR, Eddy MJ, Hout MC, Shapiro LR, Gianaros PJ (2005) A simple device to mildly stimulate the carotid baroreceptors. Psychophysiology 42(Suppl. 1):S69
  • Knecht S, Deppe M, Bäcker M, Henningsen REBH (1997) Regional cerebral blood flow increases during preparation for and processing of sensory stimuli. Exp Brain Res 116:309–314. https://doi.org/10.1007/PL00005758
  • Levine BD, Zhang R (2008) Comments on point: counterpoint: sympathetic activity does/does not influence cerebral blood flow. J Appl Physiol 105:1369–1373. https://doi.org/10.1152/japplphysiol.zdg-8199.pcpcomm.2008
  • Montoro CI, Duschek S, Reyes del Paso GA (2018) Variability in cerebral blood flow velocity at rest and during mental stress in healthy individuals: associations with cardiovascular parameters and cognitive performance. Biol Psychol 135:149–158. https://doi.org/10.1016/j.biopsycho.2018.04.005
  • Nyklíček I, Wijnen V, Rau H (2005) Effects of baroreceptor stimulation and opioids on the auditory startle reflex. Psychophysiology 42:213–222. https://doi.org/10.1111/j.1469-8986.2005.00273.x
  • Ogoh S, Tzeng Y, Lucas SJE, Galvin SD, Ainslie PN (2010) Influence of baroreflex-mediated tachycardia on the regulation of dynamic cerebral perfusion during acute hypotension in humans. J Physiol 588(2):365–371. https://doi.org/10.1113/jphysiol.2009.180844
  • Purkayastha S, Maffuid K, Zhu X, Zhang R, Ravens PB (2018) The influence of the carotid baroreflex on dynamic regulation of cerebral blood flow and cerebral tissue oxygenation in humans at rest and during exercise. Eur J Appl Physiol 118:959–969. https://doi.org/10.1007/s00421-018-3831-1
  • Querido JS, Sheel AW (2007) Regulation of cerebral blood flow during exercise. Sports Med 37:765–782. https://doi.org/10.2165/00007256-200737090-00002
  • Rau H, Pauli P, Brody S, Elbert T, Birbaumer N (1993) Baroreceptor stimulation alters cortical activity. Psychophysiology 30:322–325. https://doi.org/10.1111/j.1469-8986.1993.tb03359.x
  • Rau H, Elbert T (2001) Psychophysiology of arterial baroreceptors and the etiology of hypertension. Biol Psychol 57:179–201. https://doi.org/10.1016/S0301-0511(01)00094-1
  • Reyes del Paso GA, González MI, Hernández JA, Duschek S, Gutiérrez N (2009) Tonic blood pressure modulated the relationships between baroreceptor cardiac reflex sensitivity and cognitive performance. Psychophysiology 46:932–938. https://doi.org/10.1111/j.1469-8986.2011.01276.x
  • Reyes del Paso GA, Montoro CI, de Guevara CML, Duschek S, Jennings JR (2014) The effect of baroreceptor stimulation on pain perception depends on the elicitation of the reflex cardiovascular response: evidence of the interplay between the two branches of the baroreceptor system. Biol Psychol 101:82–90. https://doi.org/10.1016/j.biopsycho.2014.07.004
  • Reyes del Paso GA, de la Coba P, Martín-Vázquez M, Thayer JF (2017) Time domain measurement of the vascular and myocardial branches of the baroreflex: a study in physically active versus sedentary individuals. Psychophysiology 54:1528–1540. https://doi.org/10.1111/psyp.12898
  • Saeed K, Mehdi F, Houshang N, Mahmood A (2004) Cerebral blood flow velocity during a short period of carotid baroreflex stimulation in the young and middle-aged humans. Internet J Neurol. https://doi.org/10.5580/2425
  • Salinet AS, Robinson TG, Panerai RB (2013) Active, passive, and motor imagery paradigms: component analysis to assess neurovascular coupling. J Appl Physiol 114:1406–1412. https://doi.org/10.1152/japplphysiol.01448.2012
  • Thayer JF, Ahs F, Fredrikson M, Sollers JJ 3rd, Wager TD (2012) A meta-analysis of heart rate variability and neuroimaging studies: implications for heart rate variability as a marker of stress and health. Neurosci Biobehav Rev 36:747–756. https://doi.org/10.1016/j.neubiorev.2011.11.009
  • Yang SH, Liu R (2017) Cerebral autoregulation. In: Caplan LR, Biller J, Leary M, Lo E, Thomas A, Yenari M, Zhang J (eds) Primer on cerebrovascular diseases. Academic Press, New York, NY, pp 57–60