Skip to main content
Top
Published in: Neurocritical Care 3/2023

20-12-2022 | Isoflurane | Original Work

Spatial and Temporal Comparisons of Calcium Channel and Intrinsic Signal Imaging During in Vivo Cortical Spreading Depolarizations in Healthy and Hypoxic Brains

Authors: Candi L. LaSarge, Carlie McCoy, Devi V. Namboodiri, Jed A. Hartings, Steve C. Danzer, Matthew R. Batie, Jesse Skoch

Published in: Neurocritical Care | Issue 3/2023

Login to get access

Abstract

Background

Spreading depolarizations (SDs) can be viewed at a cellular level using calcium imaging (CI), but this approach is limited to laboratory applications and animal experiments. Optical intrinsic signal imaging (OISI), on the other hand, is amenable to clinical use and allows viewing of large cortical areas without contrast agents. A better understanding of the behavior of OISI-observed SDs under different brain conditions is needed.

Methods

We performed simultaneous calcium and OISI of SDs in GCaMP6f mice. SDs propagate through the cortex as a pathological wave and trigger a neurovascular response that can be imaged with both techniques. We imaged both mechanically stimulated SDs (sSDs) in healthy brains and terminal SDs (tSDs) induced by system hypoxia and cardiopulmonary failure.

Results

We observed a lag in the detection of SDs in the OISI channels compared with CI. sSDs had a faster velocity than tSDs, and tSDs had a greater initial velocity for the first 400 µm when observed with CI compared with OISI. However, both imaging methods revealed similar characteristics, including a decrease in the sSD (but not tSD) velocities as the wave moved away from the site of initial detection. CI and OISI also showed similar spatial propagation of the SD throughout the image field. Importantly, only OISI allowed regional ischemia to be detected before tSDs occurred.

Conclusions

Altogether, data indicate that monitoring either neural activity or intrinsic signals with high-resolution optical imaging can be useful to assess SDs, but OISI may be a clinically applicable way to predict, and therefore possibly mitigate, hypoxic-ischemic tSDs.
Appendix
Available only for authorised users
Literature
1.
go back to reference Leao AAP. Spreading depression of activity in the cerebral cortex. J Neurophysiol. 1944;7:359–90.CrossRef Leao AAP. Spreading depression of activity in the cerebral cortex. J Neurophysiol. 1944;7:359–90.CrossRef
2.
go back to reference Hartings JA, Andaluz N, Bullock MR, Hinzman JM, Mathern B, Pahl C, et al. Prognostic value of spreading depolarizations in patients with severe traumatic brain injury. JAMA Neurol. 2020;77:489–99.PubMedCrossRef Hartings JA, Andaluz N, Bullock MR, Hinzman JM, Mathern B, Pahl C, et al. Prognostic value of spreading depolarizations in patients with severe traumatic brain injury. JAMA Neurol. 2020;77:489–99.PubMedCrossRef
4.
go back to reference Fabricius M, Fuhr S, Willumsen L, Dreier JP, Bhatia R, Boutelle MG, et al. Association of seizures with cortical spreading depression and peri-infarct depolarisations in the acutely injured human brain. Clin Neurophysiol. 2008;119:1973–84.PubMedPubMedCentralCrossRef Fabricius M, Fuhr S, Willumsen L, Dreier JP, Bhatia R, Boutelle MG, et al. Association of seizures with cortical spreading depression and peri-infarct depolarisations in the acutely injured human brain. Clin Neurophysiol. 2008;119:1973–84.PubMedPubMedCentralCrossRef
5.
6.
go back to reference Hartings JA, Shuttleworth CW, Kirov SA, Ayata C, Hinzman JM, Foreman B, et al. The continuum of spreading depolarizations in acute cortical lesion development: examining Leão’s legacy. J Cereb Blood Flow Metab. 2017;37:1571–94.PubMedCrossRef Hartings JA, Shuttleworth CW, Kirov SA, Ayata C, Hinzman JM, Foreman B, et al. The continuum of spreading depolarizations in acute cortical lesion development: examining Leão’s legacy. J Cereb Blood Flow Metab. 2017;37:1571–94.PubMedCrossRef
7.
go back to reference De Crespigny AJ, Rother J, Beaulieu C, Moseley ME. Rapid monitoring of diffusion, DC potential, and blood oxygenation changes during global ischemia: effects of hypoglycemia, hyperglycemia, and TTX. Stroke. 1999;30(10):2212–22.PubMedCrossRef De Crespigny AJ, Rother J, Beaulieu C, Moseley ME. Rapid monitoring of diffusion, DC potential, and blood oxygenation changes during global ischemia: effects of hypoglycemia, hyperglycemia, and TTX. Stroke. 1999;30(10):2212–22.PubMedCrossRef
8.
go back to reference Risher WC, Ard D, Yuan J, Kirov SA. Recurrent spontaneous spreading depolarizations facilitate acute dendritic injury in the ischemic penumbra. J Neurosci. 2010;30:9859–68.PubMedPubMedCentralCrossRef Risher WC, Ard D, Yuan J, Kirov SA. Recurrent spontaneous spreading depolarizations facilitate acute dendritic injury in the ischemic penumbra. J Neurosci. 2010;30:9859–68.PubMedPubMedCentralCrossRef
9.
go back to reference Dreier JP, Major S, Lemale CL, Kola V, Reiffurth C, Schoknecht K, Woitzik J. Correlates of spreading depolarization, spreading depression, and negative ultraslow potential in epidural versus subdural electrocorticography. Front Neurosci. 2019;13:373.PubMedPubMedCentralCrossRef Dreier JP, Major S, Lemale CL, Kola V, Reiffurth C, Schoknecht K, Woitzik J. Correlates of spreading depolarization, spreading depression, and negative ultraslow potential in epidural versus subdural electrocorticography. Front Neurosci. 2019;13:373.PubMedPubMedCentralCrossRef
10.
go back to reference Carlson AP, Shuttleworth CW, Major S, Lemale CL, Dreier JP, Hartings JA. Terminal spreading depolarizations causing electrocortical silencing prior to clinical brain death: case report. J Neurosurg. 2018;131:1773–9.PubMedCrossRef Carlson AP, Shuttleworth CW, Major S, Lemale CL, Dreier JP, Hartings JA. Terminal spreading depolarizations causing electrocortical silencing prior to clinical brain death: case report. J Neurosurg. 2018;131:1773–9.PubMedCrossRef
11.
go back to reference Basarsky TA, Duffy SN, Andrew RD, MacVicar BA. Imaging spreading depression and associated intracellular calcium waves in brain slices. J Neurosci. 1998;18:7189–99.PubMedPubMedCentralCrossRef Basarsky TA, Duffy SN, Andrew RD, MacVicar BA. Imaging spreading depression and associated intracellular calcium waves in brain slices. J Neurosci. 1998;18:7189–99.PubMedPubMedCentralCrossRef
12.
go back to reference Teplov V, Shatillo A, Nippolainen E, Gröhn O, Giniatullin R, Kamshilin AA. Fast vascular component of cortical spreading depression revealed in rats by blood pulsation imaging. J Biomed Opt. 2014;19(4):046011.PubMedCrossRef Teplov V, Shatillo A, Nippolainen E, Gröhn O, Giniatullin R, Kamshilin AA. Fast vascular component of cortical spreading depression revealed in rats by blood pulsation imaging. J Biomed Opt. 2014;19(4):046011.PubMedCrossRef
13.
go back to reference Martin C, Martindale J, Berwick J, Mayhew J. Investigating neural-hemodynamic coupling and the hemodynamic response function in the awake rat. Neuroimage. 2006;32:33–48.PubMedCrossRef Martin C, Martindale J, Berwick J, Mayhew J. Investigating neural-hemodynamic coupling and the hemodynamic response function in the awake rat. Neuroimage. 2006;32:33–48.PubMedCrossRef
14.
go back to reference Dreier JP, Major S, Foreman B, Winkler MKL, Kang EJ, Milakara D, et al. Terminal spreading depolarization and electrical silence in death of human cerebral cortex. Ann Neurol. 2018;83:295–310.PubMedPubMedCentralCrossRef Dreier JP, Major S, Foreman B, Winkler MKL, Kang EJ, Milakara D, et al. Terminal spreading depolarization and electrical silence in death of human cerebral cortex. Ann Neurol. 2018;83:295–310.PubMedPubMedCentralCrossRef
15.
go back to reference Murphy TH, Li P, Betts K, Liu R. Two-photon imaging of stroke onset in vivo reveals that NMDA-receptor independent ischemic depolarization is the major cause of rapid reversible damage to dendrites and spines. J Neurosci. 2008;28:1756–72.PubMedPubMedCentralCrossRef Murphy TH, Li P, Betts K, Liu R. Two-photon imaging of stroke onset in vivo reveals that NMDA-receptor independent ischemic depolarization is the major cause of rapid reversible damage to dendrites and spines. J Neurosci. 2008;28:1756–72.PubMedPubMedCentralCrossRef
16.
go back to reference Takano H, Motohashi N, Uema T, Ogawa K, Ohnishi T, Nishikawa M, et al. Changes in regional cerebral blood flow during acute electroconvulsive therapy in patients with depression: positron emission tomographic study. Br J Psychiatry. 2007;190:63–8.PubMedCrossRef Takano H, Motohashi N, Uema T, Ogawa K, Ohnishi T, Nishikawa M, et al. Changes in regional cerebral blood flow during acute electroconvulsive therapy in patients with depression: positron emission tomographic study. Br J Psychiatry. 2007;190:63–8.PubMedCrossRef
17.
go back to reference De Crespigny A, Rother T, Van Bruggen N, Beaulieu C, Moseley ME. Magnetic resonance imaging assessment of cerebral hemodynamics during spreading depression in rats. J Cereb Blood Flow Metaholism. 1998;18:1008–18.CrossRef De Crespigny A, Rother T, Van Bruggen N, Beaulieu C, Moseley ME. Magnetic resonance imaging assessment of cerebral hemodynamics during spreading depression in rats. J Cereb Blood Flow Metaholism. 1998;18:1008–18.CrossRef
18.
go back to reference Van Bruggen N, Busch E, Palmer JT, Williams SP, De Crespigny AJ. High-resolution functional magnetic resonance imaging of the rat brain: mapping changes in cerebral blood volume using iron oxide contrast media. J Cereb Blood Flow Metab. 1998;18:1178–83.PubMedCrossRef Van Bruggen N, Busch E, Palmer JT, Williams SP, De Crespigny AJ. High-resolution functional magnetic resonance imaging of the rat brain: mapping changes in cerebral blood volume using iron oxide contrast media. J Cereb Blood Flow Metab. 1998;18:1178–83.PubMedCrossRef
19.
go back to reference Busch E, Gyngell ML, Eis M, Hoehn-Berlage M, Hossmann KA. Potassium-induced cortical spreading depressions during focal cerebral ischemia in rats: contribution to lesion growth assessed by diffusion-weighted NMR and biochemical imaging. J Cereb Blood Flow Metab. 1996;16:1090–9.PubMedCrossRef Busch E, Gyngell ML, Eis M, Hoehn-Berlage M, Hossmann KA. Potassium-induced cortical spreading depressions during focal cerebral ischemia in rats: contribution to lesion growth assessed by diffusion-weighted NMR and biochemical imaging. J Cereb Blood Flow Metab. 1996;16:1090–9.PubMedCrossRef
20.
go back to reference Cain SM, Bohnet B, LeDue J, Yung AC, Garcia E, Tyson JR, Snutch TP. In vivo imaging reveals that pregabalin inhibits cortical spreading depression and propagation to subcortical brain structures. Proc Nat Acad Sci. 2017;114(9):2401–6.PubMedPubMedCentralCrossRef Cain SM, Bohnet B, LeDue J, Yung AC, Garcia E, Tyson JR, Snutch TP. In vivo imaging reveals that pregabalin inhibits cortical spreading depression and propagation to subcortical brain structures. Proc Nat Acad Sci. 2017;114(9):2401–6.PubMedPubMedCentralCrossRef
21.
go back to reference Röther J, De Crespigny AJ, D’Arceuil H, Moseley ME. MR detection of cortical spreading depression immediately after focal ischemia in the rat. J Cereb Blood Flow Metab. 1996;16:214–20.PubMedCrossRef Röther J, De Crespigny AJ, D’Arceuil H, Moseley ME. MR detection of cortical spreading depression immediately after focal ischemia in the rat. J Cereb Blood Flow Metab. 1996;16:214–20.PubMedCrossRef
22.
go back to reference Fujihira M, Aoki D, Okabe Y, Takano H, Hokari H, Frommer J, Sakai F. Effect of capillary force on friction force microscopy: a scanning hydrophilicity microscope. Chem Lett. 1996;25(7):499–500.CrossRef Fujihira M, Aoki D, Okabe Y, Takano H, Hokari H, Frommer J, Sakai F. Effect of capillary force on friction force microscopy: a scanning hydrophilicity microscope. Chem Lett. 1996;25(7):499–500.CrossRef
23.
go back to reference Steffensen AB, Sword J, Croom D, Kirov SA, MacAulay N. Chloride Cotransporters as a molecular mechanism underlying spreading depolarization-induced dendritic beading. J Neurosci. 2015;35:12172–87.PubMedPubMedCentralCrossRef Steffensen AB, Sword J, Croom D, Kirov SA, MacAulay N. Chloride Cotransporters as a molecular mechanism underlying spreading depolarization-induced dendritic beading. J Neurosci. 2015;35:12172–87.PubMedPubMedCentralCrossRef
24.
go back to reference Van Harreveld A, Khattab FI. Changes in cortical extracellular space during spreading depression investigated with the electron microscope. J Neurophysiol. 1967;30:911–29.PubMedCrossRef Van Harreveld A, Khattab FI. Changes in cortical extracellular space during spreading depression investigated with the electron microscope. J Neurophysiol. 1967;30:911–29.PubMedCrossRef
25.
go back to reference Dreier JP, Reiffurth C. Exploitation of the spreading depolarization-induced cytotoxic edema for high-resolution, 3D mapping of its heterogeneous propagation paths. Proc Natl Acad Sci. 2017;114(9):2112–4.PubMedPubMedCentralCrossRef Dreier JP, Reiffurth C. Exploitation of the spreading depolarization-induced cytotoxic edema for high-resolution, 3D mapping of its heterogeneous propagation paths. Proc Natl Acad Sci. 2017;114(9):2112–4.PubMedPubMedCentralCrossRef
26.
go back to reference Thijs VN, Lansberg MG, Beaulieu C, Marks MP, Moseley ME, Albers GW. Is early ischemic lesion volume on diffusion-weighted imaging an independent predictor of stroke outcome? A multivariable analysis. Stroke. 2000;31:2597–602.PubMedCrossRef Thijs VN, Lansberg MG, Beaulieu C, Marks MP, Moseley ME, Albers GW. Is early ischemic lesion volume on diffusion-weighted imaging an independent predictor of stroke outcome? A multivariable analysis. Stroke. 2000;31:2597–602.PubMedCrossRef
27.
go back to reference Feuerstein D, Manning A, Hashemi P, Bhatia R, Fabricius M, Tolias C, Boutelle MG. Dynamic metabolic response to multiple spreading depolarizations in patients with acute brain injury: an online microdialysis study. J Cereb Blood Flow Metab. 2010;30(7):1343–55.PubMedPubMedCentralCrossRef Feuerstein D, Manning A, Hashemi P, Bhatia R, Fabricius M, Tolias C, Boutelle MG. Dynamic metabolic response to multiple spreading depolarizations in patients with acute brain injury: an online microdialysis study. J Cereb Blood Flow Metab. 2010;30(7):1343–55.PubMedPubMedCentralCrossRef
28.
go back to reference Hashemi P, Dankoski EC, Petrovic J, Keithley RB, Wightman R. Voltammetric detection of 5-Hydroxytryptamine release in the rat brain. Anal Chem. 2009;81(22):9462–71.PubMedPubMedCentralCrossRef Hashemi P, Dankoski EC, Petrovic J, Keithley RB, Wightman R. Voltammetric detection of 5-Hydroxytryptamine release in the rat brain. Anal Chem. 2009;81(22):9462–71.PubMedPubMedCentralCrossRef
29.
go back to reference Strong AJ, Hartings JA, Dreier JP. Cortical spreading depression: an adverse but treatable factor in intensive care? Curr Opin Crit Care. 2007;13:126–33.PubMedCrossRef Strong AJ, Hartings JA, Dreier JP. Cortical spreading depression: an adverse but treatable factor in intensive care? Curr Opin Crit Care. 2007;13:126–33.PubMedCrossRef
30.
go back to reference Woitzik J, Hecht N, Pinczolits A, Sandow N, Major S, Winkler MKL, et al. Propagation of cortical spreading depolarization in the human cortex after malignant stroke. Neurology. 2013;80:1095–102.PubMedCrossRef Woitzik J, Hecht N, Pinczolits A, Sandow N, Major S, Winkler MKL, et al. Propagation of cortical spreading depolarization in the human cortex after malignant stroke. Neurology. 2013;80:1095–102.PubMedCrossRef
31.
go back to reference Klatzo I. Presidental address. Neuropathological aspects of brain edema. J Neuropathol Exp Neurol. 1967;26:1–14.PubMedCrossRef Klatzo I. Presidental address. Neuropathological aspects of brain edema. J Neuropathol Exp Neurol. 1967;26:1–14.PubMedCrossRef
32.
33.
go back to reference Bogdanov VB, Middleton NA, Theriot JJ, Parker PD, Abdullah OM, Ju YS, et al. Susceptibility of primary sensory cortex to spreading depolarizations. J Neurosci. 2016;36:4733–43.PubMedPubMedCentralCrossRef Bogdanov VB, Middleton NA, Theriot JJ, Parker PD, Abdullah OM, Ju YS, et al. Susceptibility of primary sensory cortex to spreading depolarizations. J Neurosci. 2016;36:4733–43.PubMedPubMedCentralCrossRef
34.
go back to reference Grinvald A, Lieke E, Frostig RD, Gilbert CD, Wiesel TN. Functional architecture of cortex revealed by optical imaging of intrinsic signals. Nature. 1986;324:361–4.PubMedCrossRef Grinvald A, Lieke E, Frostig RD, Gilbert CD, Wiesel TN. Functional architecture of cortex revealed by optical imaging of intrinsic signals. Nature. 1986;324:361–4.PubMedCrossRef
35.
go back to reference Ma H, Zhao M, Schwartz TH. Dynamic neurovascular coupling and uncoupling during ictal onset, propagation, and termination revealed by simultaneous in vivo optical imaging of neural activity and local blood volume. Cereb Cortex. 2013;23:885–99.PubMedCrossRef Ma H, Zhao M, Schwartz TH. Dynamic neurovascular coupling and uncoupling during ictal onset, propagation, and termination revealed by simultaneous in vivo optical imaging of neural activity and local blood volume. Cereb Cortex. 2013;23:885–99.PubMedCrossRef
36.
go back to reference Ma Y, Shaik MA, Kim SH, Kozberg MG, Thibodeaux DN, Zhao HT, et al. Wide-field optical mapping of neural activity and brain haemodynamics: considerations and novel approaches. Philos Trans R Soc Lond B Biol Sci. 2016;371:20150360.PubMedPubMedCentralCrossRef Ma Y, Shaik MA, Kim SH, Kozberg MG, Thibodeaux DN, Zhao HT, et al. Wide-field optical mapping of neural activity and brain haemodynamics: considerations and novel approaches. Philos Trans R Soc Lond B Biol Sci. 2016;371:20150360.PubMedPubMedCentralCrossRef
37.
go back to reference Farkas E, Bari F, Obrenovitch TP. Multi-modal imaging of anoxic depolarization and hemodynamic changes induced by cardiac arrest in the rat cerebral cortex. Neuroimage. 2010;51:734–42.PubMedCrossRef Farkas E, Bari F, Obrenovitch TP. Multi-modal imaging of anoxic depolarization and hemodynamic changes induced by cardiac arrest in the rat cerebral cortex. Neuroimage. 2010;51:734–42.PubMedCrossRef
38.
go back to reference Haglund MM, Ojemann GA, Hochman DW. Optical imaging of epileptiform and functional activity in human cerebral cortex. Nature. 1992;358:668–71.PubMedCrossRef Haglund MM, Ojemann GA, Hochman DW. Optical imaging of epileptiform and functional activity in human cerebral cortex. Nature. 1992;358:668–71.PubMedCrossRef
39.
go back to reference Hillman EMC. Optical brain imaging in vivo: techniques and applications from animal to man. J Biomed Opt. 2007;12:051402.PubMedCrossRef Hillman EMC. Optical brain imaging in vivo: techniques and applications from animal to man. J Biomed Opt. 2007;12:051402.PubMedCrossRef
40.
go back to reference Hallum LE, Chen SC, Cloherty SL, Morley JW, Suaning GJ, Lovell NH. Functional optical imaging of intrinsic signals in cerebral cortex. Wiley Encycl Biomed Eng. Hoboken, NJ, USA: John Wiley & Sons, Inc.; 2006. p. 1–8. Hallum LE, Chen SC, Cloherty SL, Morley JW, Suaning GJ, Lovell NH. Functional optical imaging of intrinsic signals in cerebral cortex. Wiley Encycl Biomed Eng. Hoboken, NJ, USA: John Wiley & Sons, Inc.; 2006. p. 1–8.
41.
go back to reference Villringer A, Chance B. Non-invasive optical spectroscopy and imaging of human brain function. Trends Neurosci. 1997;20:435–42.PubMedCrossRef Villringer A, Chance B. Non-invasive optical spectroscopy and imaging of human brain function. Trends Neurosci. 1997;20:435–42.PubMedCrossRef
42.
go back to reference Hewson-Stoate N, Jones M, Martindale J, Berwick J, Mayhew J. Further nonlinearities in neurovascular coupling in rodent barrel cortex. Neuroimage. 2005;24:565–74.PubMedCrossRef Hewson-Stoate N, Jones M, Martindale J, Berwick J, Mayhew J. Further nonlinearities in neurovascular coupling in rodent barrel cortex. Neuroimage. 2005;24:565–74.PubMedCrossRef
43.
go back to reference Obrenovitch TP, Chen S, Farkas E. Simultaneous, live imaging of cortical spreading depression and associated cerebral blood flow changes, by combining voltage-sensitive dye and laser speckle contrast methods. Neuroimage. 2009;45:68–74.PubMedCrossRef Obrenovitch TP, Chen S, Farkas E. Simultaneous, live imaging of cortical spreading depression and associated cerebral blood flow changes, by combining voltage-sensitive dye and laser speckle contrast methods. Neuroimage. 2009;45:68–74.PubMedCrossRef
44.
go back to reference Suh M, Ma H, Zhao M, Sharif S, Schwartz TH. Neurovascular coupling and oximetry during epileptic events. Mol Neurobiol. 2006;33:181–97.PubMedCrossRef Suh M, Ma H, Zhao M, Sharif S, Schwartz TH. Neurovascular coupling and oximetry during epileptic events. Mol Neurobiol. 2006;33:181–97.PubMedCrossRef
45.
go back to reference Siegel F, Lohmann C. Probing synaptic function in dendrites with calcium imaging. Exp Neurol. 2013;242:27–32.PubMedCrossRef Siegel F, Lohmann C. Probing synaptic function in dendrites with calcium imaging. Exp Neurol. 2013;242:27–32.PubMedCrossRef
46.
go back to reference Dana H, Chen T-W, Hu A, Shields BC, Guo C, Looger LL, et al. Thy1-GCaMP6 transgenic mice for neuronal population imaging in vivo. PLoS ONE. 2014;9:e108697.PubMedPubMedCentralCrossRef Dana H, Chen T-W, Hu A, Shields BC, Guo C, Looger LL, et al. Thy1-GCaMP6 transgenic mice for neuronal population imaging in vivo. PLoS ONE. 2014;9:e108697.PubMedPubMedCentralCrossRef
47.
go back to reference Raymond SB, Skoch J, Hynynen K, Bacskai BJ. Multiphoton imaging of ultrasound/Optison mediated cerebrovascular effects in vivo. J Cereb Blood Flow Metab. 2007;27:393–403.PubMedCrossRef Raymond SB, Skoch J, Hynynen K, Bacskai BJ. Multiphoton imaging of ultrasound/Optison mediated cerebrovascular effects in vivo. J Cereb Blood Flow Metab. 2007;27:393–403.PubMedCrossRef
48.
go back to reference Heo C, Park H, Kim Y-T, Baeg E, Kim YH, Kim S-G, et al. A soft, transparent, freely accessible cranial window for chronic imaging and electrophysiology. Sci Rep. 2016;6:27818.PubMedPubMedCentralCrossRef Heo C, Park H, Kim Y-T, Baeg E, Kim YH, Kim S-G, et al. A soft, transparent, freely accessible cranial window for chronic imaging and electrophysiology. Sci Rep. 2016;6:27818.PubMedPubMedCentralCrossRef
49.
go back to reference O’Farrell AM, Rex DE, Muthialu A, Pouratian N, Wong GK, Cannestra AF, et al. Characterization of optical intrinsic signals and blood volume during cortical spreading depression. NeuroReport. 2000;11:2121–5.PubMedCrossRef O’Farrell AM, Rex DE, Muthialu A, Pouratian N, Wong GK, Cannestra AF, et al. Characterization of optical intrinsic signals and blood volume during cortical spreading depression. NeuroReport. 2000;11:2121–5.PubMedCrossRef
50.
go back to reference Ba AM, Guiou M, Pouratian N, Muthialu A, Rex DE, Cannestra AF, et al. Multiwavelength optical intrinsic signal imaging of cortical spreading depression. J Neurophysiol. 2002;88:2726–35.PubMedCrossRef Ba AM, Guiou M, Pouratian N, Muthialu A, Rex DE, Cannestra AF, et al. Multiwavelength optical intrinsic signal imaging of cortical spreading depression. J Neurophysiol. 2002;88:2726–35.PubMedCrossRef
51.
go back to reference Bures J, Bureš J, Buresova O, Bures̆ová, O., Křivánek, J., & Krivanek, J. The mechanism and applications of Leao’s spreading depression of electroencephalographic activity. Cambridge: Academic Press; 1974. Bures J, Bureš J, Buresova O, Bures̆ová, O., Křivánek, J., & Krivanek, J. The mechanism and applications of Leao’s spreading depression of electroencephalographic activity. Cambridge: Academic Press; 1974.
52.
go back to reference Dreier JP, Woitzik J, Fabricius M, Bhatia R, Major S, Drenckhahn C, Strong AJ. Delayed ischaemic neurological deficits after subarachnoid haemorrhage are associated with clusters of spreading depolarizations. Brain. 2006;129(12):3224–37.PubMedCrossRef Dreier JP, Woitzik J, Fabricius M, Bhatia R, Major S, Drenckhahn C, Strong AJ. Delayed ischaemic neurological deficits after subarachnoid haemorrhage are associated with clusters of spreading depolarizations. Brain. 2006;129(12):3224–37.PubMedCrossRef
53.
go back to reference Milakara D, Grozea C, Dahlem M, Major S, Winkler MK, Lückl J, Dreier JP. Simulation of spreading depolarization trajectories in cerebral cortex correlation of velocity and susceptibility in patients with aneurysmal subarachnoid hemorrhage. NeuroImage Clin. 2017;16:524–38.PubMedPubMedCentralCrossRef Milakara D, Grozea C, Dahlem M, Major S, Winkler MK, Lückl J, Dreier JP. Simulation of spreading depolarization trajectories in cerebral cortex correlation of velocity and susceptibility in patients with aneurysmal subarachnoid hemorrhage. NeuroImage Clin. 2017;16:524–38.PubMedPubMedCentralCrossRef
54.
go back to reference Brennan KC, Beltrán-Parrazal L, López-Valdés HE, Theriot J, Toga AW, Charles AC. Distinct vascular conduction with cortical spreading depression. J Neurophysiol. 2007;97:4143–51.PubMedCrossRef Brennan KC, Beltrán-Parrazal L, López-Valdés HE, Theriot J, Toga AW, Charles AC. Distinct vascular conduction with cortical spreading depression. J Neurophysiol. 2007;97:4143–51.PubMedCrossRef
55.
go back to reference Tsien RY. A non-disruptive technique for loading calcium buffers and indicators into cells. Nature. 1981;290:527–8.PubMedCrossRef Tsien RY. A non-disruptive technique for loading calcium buffers and indicators into cells. Nature. 1981;290:527–8.PubMedCrossRef
56.
go back to reference Takahashi N, Sasaki T, Usami A, Matsuki N, Ikegaya Y. Watching neuronal circuit dynamics through functional multineuron calcium imaging (fMCI). Neurosci Res. 2007;58:219–25.PubMedCrossRef Takahashi N, Sasaki T, Usami A, Matsuki N, Ikegaya Y. Watching neuronal circuit dynamics through functional multineuron calcium imaging (fMCI). Neurosci Res. 2007;58:219–25.PubMedCrossRef
57.
go back to reference Santos E, Schöll M, Sánchez-Porras R, Dahlem MA, Silos H, Unterberg A, et al. Radial, spiral and reverberating waves of spreading depolarization occur in the gyrencephalic brain. Neuroimage. 2014;99:244–55.PubMedCrossRef Santos E, Schöll M, Sánchez-Porras R, Dahlem MA, Silos H, Unterberg A, et al. Radial, spiral and reverberating waves of spreading depolarization occur in the gyrencephalic brain. Neuroimage. 2014;99:244–55.PubMedCrossRef
58.
59.
60.
go back to reference Taş YÇ, Solaroğlu İ, Gürsoy-Özdemir Y. Spreading depolarization waves in neurological diseases: a short review about its pathophysiology and clinical relevance. Curr Neuropharmacol. 2019;17:151–64.PubMedPubMedCentralCrossRef Taş YÇ, Solaroğlu İ, Gürsoy-Özdemir Y. Spreading depolarization waves in neurological diseases: a short review about its pathophysiology and clinical relevance. Curr Neuropharmacol. 2019;17:151–64.PubMedPubMedCentralCrossRef
61.
go back to reference Devor A, Ulbert I, Dunn AK, Narayanan SN, Jones SR, Andermann ML, et al. Coupling of the cortical hemodynamic response to cortical and thalamic neuronal activity. Proc Natl Acad Sci. 2005;102:3822–7.PubMedPubMedCentralCrossRef Devor A, Ulbert I, Dunn AK, Narayanan SN, Jones SR, Andermann ML, et al. Coupling of the cortical hemodynamic response to cortical and thalamic neuronal activity. Proc Natl Acad Sci. 2005;102:3822–7.PubMedPubMedCentralCrossRef
62.
go back to reference Logothetis NK, Pauls J, Augath M, Trinath T, Oeltermann A. Neurophysiological investigation of the basis of the fMRI signal. Nature. 2001;412:150–7.PubMedCrossRef Logothetis NK, Pauls J, Augath M, Trinath T, Oeltermann A. Neurophysiological investigation of the basis of the fMRI signal. Nature. 2001;412:150–7.PubMedCrossRef
63.
go back to reference Oliveira-Ferreira AI, Milakara D, Alam M, Jorks D, Major S, Hartings JA, et al. Experimental and preliminary clinical evidence of an ischemic zone with prolonged negative DC shifts surrounded by a normally perfused tissue belt with persistent electrocorticographic depression. J Cereb Blood Flow Metab. 2010;30:1504–19.PubMedPubMedCentralCrossRef Oliveira-Ferreira AI, Milakara D, Alam M, Jorks D, Major S, Hartings JA, et al. Experimental and preliminary clinical evidence of an ischemic zone with prolonged negative DC shifts surrounded by a normally perfused tissue belt with persistent electrocorticographic depression. J Cereb Blood Flow Metab. 2010;30:1504–19.PubMedPubMedCentralCrossRef
64.
go back to reference Busija DW, Bari F, Domoki F, Horiguchi T, Shimizu K. Mechanisms involved in the cerebrovascular dilator effects of cortical spreading depression. Prog Neurobiol. 2008;86:417–33.PubMedCentralCrossRef Busija DW, Bari F, Domoki F, Horiguchi T, Shimizu K. Mechanisms involved in the cerebrovascular dilator effects of cortical spreading depression. Prog Neurobiol. 2008;86:417–33.PubMedCentralCrossRef
65.
go back to reference von Bornstädt D, Houben T, Seidel JL, Zheng Y, Dilekoz E, Qin T, et al. Supply-demand mismatch transients in susceptible peri-infarct hot zones explain the origins of spreading injury depolarizations. Neuron. 2015;85:1117–31.CrossRef von Bornstädt D, Houben T, Seidel JL, Zheng Y, Dilekoz E, Qin T, et al. Supply-demand mismatch transients in susceptible peri-infarct hot zones explain the origins of spreading injury depolarizations. Neuron. 2015;85:1117–31.CrossRef
Metadata
Title
Spatial and Temporal Comparisons of Calcium Channel and Intrinsic Signal Imaging During in Vivo Cortical Spreading Depolarizations in Healthy and Hypoxic Brains
Authors
Candi L. LaSarge
Carlie McCoy
Devi V. Namboodiri
Jed A. Hartings
Steve C. Danzer
Matthew R. Batie
Jesse Skoch
Publication date
20-12-2022
Publisher
Springer US
Keyword
Isoflurane
Published in
Neurocritical Care / Issue 3/2023
Print ISSN: 1541-6933
Electronic ISSN: 1556-0961
DOI
https://doi.org/10.1007/s12028-022-01660-7

Other articles of this Issue 3/2023

Neurocritical Care 3/2023 Go to the issue