nach oben

Brain Structure and Function

Erschienen in:

10.09.2018 | Original Article

Activation in the auditory pathway of the gerbil studied with ¹⁸F-FDG PET: effects of anesthesia

verfasst von: M. Kessler, M. Mamach, R. Beutelmann, J. P. Bankstahl, F. M. Bengel, G. M. Klump, Georg Berding

Erschienen in: Brain Structure and Function | Ausgabe 9/2018

Einloggen, um Zugang zu erhalten

Abstract

Here, we present results from an ¹⁸F-fluorodeoxyglucose (¹⁸F-FDG) positron emission tomography (PET) study in the Mongolian gerbil, a preferred animal model in auditory research. One major issue in preclinical nuclear imaging, as well as in most of the neurophysiological methods investigating auditory processing, is the need of anesthesia. We compared the usability of two types of anesthesia which are frequently employed in electrophysiology, ketamine/xylazine (KX), and fentanyl/midazolam/medetomidine (FMM), for valid measurements of auditory activation with ¹⁸F-FDG PET. Gerbils were placed in a sound-shielding box and injected with ¹⁸F-FDG. Two acoustic free-field conditions were used: (1) baseline (no stimulation, 25 dB background noise) and (2) 90 dB frequency-modulated tones (FM). After 40 min of ¹⁸F-FDG uptake, a 30 min acquisition was performed using a small animal PET/CT system. Blood glucose levels were measured after the uptake phase before scanning. Standardized uptake value ratios for relevant regions were determined after implementing image and volume of interest templates. Scans demonstrated a significantly higher uptake in the inferior colliculus with FM stimulation compared to baseline in awake subjects (+ 12%; p = 0.02) and with FMM anesthesia (+ 13%; p = 0.0012), but not with KX anesthesia. In non-auditory brain regions, no significant difference was detected. Blood glucose levels were significantly higher under KX compared to FMM anesthesia (17.29 ± 0.42 mmol/l vs. 14.30 ± 1.91 mmol/l; p = 0.024). These results suggest that valid ¹⁸F-FDG PET measurements of auditory activation comparable to electrophysiology can be obtained from gerbils during opioid-based anesthesia due to its limited effects on interfering blood glucose levels.

Nur mit Berechtigung zugänglich

Abdel el Motal SM, Sharp GW (1985) Inhibition of glucose-induced insulin release by xylazine. Endocrinology 116:2337–2340. https://doi.org/10.1210/endo-116-6-2337 CrossRef

Alan RP, Adrian R, Manuel SM, Troy AH (2010) Structural organization of the ascending auditory pathway. Oxford University Press, Oxford. https://doi.org/10.1093/oxfordhb/9780199233281.013.0002 CrossRef

Astl J, Popelar J, Kvasnak E, Syka J (1996) Comparison of response properties of neurons in the inferior colliculus of guinea pigs under different anesthetics. Audiology 35:335–345CrossRef

Bäuerle P, von der Behrens W, Kössl M, Gaese BH (2011) Stimulus-specific adaptation in the gerbil primary auditory thalamus is the result of a fast frequency-specific habituation and is regulated by the corticofugal system. J Neurosci 31(26):9708CrossRef

Belliveau LAC, Lyamzin DR, Lesica NA (2014) The neural representation of interaural time differences in gerbils is transformed from midbrain to cortex. J Neurosci 34:16796–16808. https://doi.org/10.1523/jneurosci.2432-14.2014 CrossRefPubMedPubMedCentral

Berding G, Wilke F, Rode T, Haense C, Joseph G, Meyer GJ, Mamach M, Lenarz M, Geworski L, Bengel FM, Lenarz T, Lim HH (2015) Positron emission tomography imaging reveals auditory and frontal cortical regions involved with speech perception and loudness adaptation. PLoS One 10:e0128743. https://doi.org/10.1371/journal.pone.0128743 CrossRefPubMedPubMedCentral

Berti V, Mosconi L, Pupi A (2014) Brain: normal variations and benign findings in FDG PET/CT imaging. PET clin 9:129–140. https://doi.org/10.1016/j.cpet.2013.10.006 CrossRefPubMed

Bizley JK, Walker KMM, Silverman BW, King AJ, Schnupp JWH (2009) Interdependent encoding of pitch, timbre, and spatial location in auditory cortex. J Neurosci 29:2064–2075. https://doi.org/10.1523/jneurosci.4755-08.2009 CrossRefPubMedPubMedCentral

Bonhomme V, Boveroux P, Hans P, Brichant JF, Vanhaudenhuyse A, Boly M, Laureys S (2011) Influence of anesthesia on cerebral blood flow, cerebral metabolic rate, and brain functional connectivity. Curr Opin Anaesthesiol 24:474–479. https://doi.org/10.1097/aco.0b013e32834a12a1 CrossRefPubMed

Brown ET, Umino Y, Loi T, Solessio E, Barlow R (2005) Anesthesia can cause sustained hyperglycemia in C57/BL6J mice. Vis Neurosci 22:615–618. https://doi.org/10.1017/S0952523805225105 CrossRefPubMed

Budinger E, Heil P, Scheich H (2000a) Functional organization of auditory cortex in the Mongolian gerbil (Meriones unguiculatus). III. Anatomical subdivisions and corticocortical connections. Eur J Neurosci 12(7):2425–2451CrossRef

Budinger E, Heil P, Scheich H (2000b) Functional organization of auditory cortex in the Mongolian gerbil (Meriones unguiculatus). IV. Connections with anatomically characterized subcortical structures. Eur J Neurosci 12(7):2452–2474CrossRef

Cant NB, Benson CG (2005) An atlas of the inferior colliculus of the gerbil in three dimensions. Hear Res 206:12–27. https://doi.org/10.1016/j.heares.2005.02.014 CrossRefPubMed

Cant NB, Benson CG (2008) Organization of the inferior colliculus of the gerbil (Meriones unguiculatus): projections from the cochlear nucleus. Neuroscience 154:206–217. https://doi.org/10.1016/j.neuroscience.2008.02.015 CrossRefPubMedPubMedCentral

Catalan-Ahumada M, Deggouj N, De Volder A, Melin J, Michel C, Veraart C (1993) High metabolic activity demonstrated by positron emission tomography in human auditory cortex in case of deafness of early onset. Brain res 623:287–292CrossRef

Chatziioannou AF (2005) Instrumentation for molecular imaging in preclinical research: Micro-PET and Micro-SPECT. Proc Am Thorac Soc 2:533–536. https://doi.org/10.1513/pats.200508-079DS (510–511)CrossRefPubMedPubMedCentral

Cheal M (1986) The gerbil: a unique model for research on aging. Exp Aging Res 12:3–21. https://doi.org/10.1080/03610738608259430 CrossRefPubMed

Coez A, Zilbovicius M, Ferrary E, Bouccara D, Mosnier I, Ambert-Dahan E, Kalamarides M, Bizaguet E, Syrota A, Samson Y, Sterkers O (2009) Processing of voices in deafness rehabilitation by auditory brainstem implant. NeuroImage 47:1792–1796. https://doi.org/10.1016/j.neuroimage.2009.05.053 CrossRefPubMed

Constantinescu CC, Mukherjee J (2009) Performance evaluation of an Inveon PET preclinical scanner. Phys Med Biol 54:2885–2899. https://doi.org/10.1088/0031-9155/54/9/020 CrossRefPubMedPubMedCentral

Dunn JT, Anthony K, Amiel SA, Marsden PK (2009) Correction for the effect of rising plasma glucose levels on quantification of MRglc with FDG-PET. J Cereb Blood Flow Metab 29:1059–1067. https://doi.org/10.1038/jcbfm.2009.21 CrossRefPubMed

Fink BR, Haschke RH (1973) Anesthetic effects on cerebral metabolism. Anesthesiology 39:199–215CrossRef

Geven LI, de Kleine E, Willemsen AT, van Dijk P (2014) Asymmetry in primary auditory cortex activity in tinnitus patients and controls. Neuroscience 256:117–125. https://doi.org/10.1016/j.neuroscience.2013.10.015 CrossRefPubMed

Giraud A-L, Truy E, Frackowiak RSJ, Grégoire M-C, Pujol J-F, Collet L (2000) Differential recruitment of the speech processing system in healthy subjects and rehabilitated cochlear implant patients. Brain 123:1391–1402. https://doi.org/10.1093/brain/123.7.1391 CrossRefPubMed

Gleich O, Strutz J (2002) Age dependent changes in the medial nucleus of the trapezoid body in gerbils. Hear Res 164:166–178. https://doi.org/10.1016/S0378-5955(01)00430-0 CrossRefPubMed

Graña GD, Hutson KA, Badea A, Pappa A, Scott W, Fitzpatrick DC (2017) The organization of frequency and binaural cues in the gerbil inferior colliculus. J Comp Neurol 525:2050–2074. https://doi.org/10.1002/cne.24155 CrossRefPubMedPubMedCentral

Green KMJ, Julyan PJ, Hastings DL, Ramsden RT (2011) Cortical activations in sequential bilateral cochlear implant users. Cochlear Implants Int 12:3–9. https://doi.org/10.1179/146701010X486507 CrossRefPubMed

Grothe B, Pecka M, McAlpine D (2010) Mechanisms of sound localization in mammals. Physiol Rev 90:983–1012. https://doi.org/10.1152/physrev.00026.2009 CrossRefPubMed

Hamann I, Gleich O, Klump GM, Kittel MC, Boettcher FA, Schmiedt RA, Strutz J (2002) Behavioral and evoked-potential thresholds in young and old Mongolian gerbils (Meriones unguiculatus). Hear Res 171:82–95. https://doi.org/10.1016/S0378-5955(02)00454-9 CrossRefPubMed

Hromádka T, Zador AM (2009) Representations in auditory cortex. Curr Opin Neurobiol 19:430–433. https://doi.org/10.1016/j.conb.2009.07.009 CrossRefPubMedPubMedCentral

Hsu WC, Tzen K-Y, Huy PTB, Duet M, Yeh TH (2009) An animal model of central auditory pathway imaging in the rat brain by high resolution small animal positron emission tomography. Acta Otolaryngol 129:423–428. https://doi.org/10.1080/00016480802593497 CrossRefPubMed

Huang SC (2000) Anatomy of SUV. Nucl Med Biol 27:643–646. https://doi.org/10.1016/S0969-8051(00)00155-4 CrossRefPubMed

Huet A, Batrel C, Tang Y, Desmadryl G, Wang J, Puel J-L, Bourien J (2016) Sound coding in the auditory nerve of gerbils. Hear Res 338:32–39. https://doi.org/10.1016/j.heares.2016.05.006 CrossRefPubMed

Ishizu K, Nishizawa S, Yonekura Y, Sadato N, Magata Y, Tamaki N, Tsuchida T, Okazawa H, Miyatake S-i, Ishikawa M (1994) Effects of hyperglycemia on FDG uptake in human brain and glioma. J Nucl Med 35:1104–1109PubMed

Jang DP, Lee KM, Lee SY, Oh JH, Park CW, Kim IY, Kim YB, Cho ZH (2012) Auditory adaptation to sound intensity in conscious rats: 2-[F-18]-fluoro-2-deoxy-d-glucose PET study. Neuroreport 23:228–233. https://doi.org/10.1097/wnr.0b013e32835022c7 CrossRefPubMed

Johnsrude IS, Giraud AL, Frackowiak RSJ (2002) Functional imaging of the auditory system: the use of positron emission tomography. Audiol Neurootol 7:251–276CrossRef

Kilbourn MR (2017) Small molecule PET tracers for transporter imaging. Semin Nucl Med 47:536–552. https://doi.org/10.1053/j.semnuclmed.2017.05.005 CrossRefPubMed

Knoop BO, Geworski L, Hofmann M, Munz DL, Knapp WH (2002) Use of recovery coefficients as a test of system linearity of response in positron emission tomography (PET). Phys Med Biol 47(8):1237–1254CrossRef

Langguth B, Eichhammer P, Kreutzer A, Maenner P, Marienhagen J, Kleinjung T, Sand P, Hajak G (2006) The impact of auditory cortex activity on characterizing and treating patients with chronic tinnitus—first results from a PET study. Acta Otolaryngol Suppl 556:84–88. https://doi.org/10.1080/03655230600895317 CrossRef

Lee JS, Lee DS, Oh SH, Kim CS, Kim JW, Hwang CH, Koo J, Kang E, Chung JK, Lee MC (2003) PET evidence of neuroplasticity in adult auditory cortex of postlingual deafness. J Nucl Med 44:1435–1439PubMed

Lesica NA, Grothe B (2008a) Dynamic spectrotemporal feature selectivity in the auditory midbrain. J Neurosci 28:5412CrossRef

Lesica NA, Grothe B (2008b) Efficient temporal processing of naturalistic sounds. PLoS One 3:e1655. https://doi.org/10.1371/journal.pone.0001655 CrossRefPubMedPubMedCentral

Meyer AF, Diepenbrock J-P, Ohl FW, Anemüller J (2014a) Temporal variability of spectro-temporal receptive fields in the anesthetized auditory cortex. Front Comput Neurosci 8:165. https://doi.org/10.3389/fncom.2014.00165 CrossRefPubMedPubMedCentral

Meyer AF, Diepenbrock JP, Happel MF, Ohl FW, Anemuller J (2014b) Discriminative learning of receptive fields from responses to non-Gaussian stimulus ensembles. PLoS One 9:e93062. https://doi.org/10.1371/journal.pone.0093062 CrossRefPubMedPubMedCentral

Mills JH, Schmiedt RA, Kulish LF (1990) Age-related changes in auditory potentials of mongolian gerbil. Hear Res 46:201–210. https://doi.org/10.1016/0378-5955(90)90002-7 CrossRefPubMed

Nelken I (2004) Processing of complex stimuli and natural scenes in the auditory cortex. Cur Opin Neurobiol 14:474–480. https://doi.org/10.1016/j.conb.2004.06.005 CrossRef

Ohl FW, Schulze H, Scheich H, Freeman WJ (2000) Spatial representation of frequency-modulated tones in gerbil auditory cortex revealed by epidural electrocorticography. J Physiol Paris 94:549–554CrossRef

Okuda T, Nagamachi S, Ushisako Y, Tono T (2013) Glucose metabolism in the primary auditory cortex of postlingually deaf patients: an FDG-PET study. ORL J Otorhinolaryngol Relat Spec 75:342–349. https://doi.org/10.1159/000357474 CrossRefPubMed

Osmanski MS, Wang X (2015) Behavioral dependence of auditory cortical responses. Brain Topogr 28:365–378. https://doi.org/10.1007/s10548-015-0428-4 CrossRefPubMedPubMedCentral

Pachitariu M, Lyamzin DR, Sahani M, Lesica NA (2015) State-dependent population coding in primary auditory cortex. J Neurosci 35:2058–2073. https://doi.org/10.1523/jneurosci.3318-14.2015 CrossRefPubMedPubMedCentral

Palmer AR, Jiang D, McAlpine D (2000) Neural responses in the inferior colliculus to binaural masking level differences created by inverting the noise in one ear. J Neurophysiol 84:844–852CrossRef

Palmer AR, Shackleton TM, Sumner CJ, Zobay O, Rees A (2013) Classification of frequency response areas in the inferior colliculus reveals continua not discrete classes. J Physiol 591:4003–4025. https://doi.org/10.1113/jphysiol.2013.255943 CrossRefPubMedPubMedCentral

Radtke-Schuller S, Schuller G, Angenstein F, Grosser OS, Goldschmidt J, Budinger E (2016) Brain atlas of the Mongolian gerbil (Meriones unguiculatus) in CT/MRI-aided stereotaxic coordinates. Brain Struct Funct 221(Suppl 1):1–272. https://doi.org/10.1007/s00429-016-1259-0 CrossRefPubMedPubMedCentral

Rauschecker JP, Tian B, Hauser M (1995) Processing of complex sounds in the macaque nonprimary auditory cortex. Science 268:111–114CrossRef

Riemann B, Schafers KP, Schober O, Schafers M (2008) Small animal PET in preclinical studies: opportunities and challenges. Q J Nucl Med Mol Imaging 52:215–221PubMed

Ryan A (1976) Hearing sensitivity of the mongolian gerbil, Meriones unguiculatis. J Acoust Soc Am 59:1222–1226CrossRef

Ryan AF, Woolf NK, Sharp FR (1982) Tonotopic organization in the central auditory pathway of the Mongolian gerbil: a 2-deoxyglucose study. J Comp Neurol 207(4):369–380. https://doi.org/10.1002/cne.902070408 CrossRefPubMed

Saha JK, Xia J, Grondin JM, Engle SK, Jakubowski JA (2005) Acute hyperglycemia induced by ketamine/xylazine anesthesia in rats: mechanisms and implications for preclinical models. Exp Biol Med (Maywood) 230:777–784CrossRef

Sanes DH, Malone BJ, Semple MN (1998) Role of synaptic inhibition in processing of dynamic binaural levelstimuli. J Neurosci 18:794–803CrossRef

Scheich H, Zuschratter W (1995) Mapping of stimulus features and meaning in gerbil auditory cortex with 2-deoxyglucose and c-Fos antibodies. Behav Brain Res 66:195–205CrossRef

Scheich H, Heil P, Langner G (1993) Functional organization of auditory cortex in the Mongolian gerbil (Meriones unguiculatus) II. Tonotopic 2-Deoxyglucose. Eur J Neurosci 5:898–914. https://doi.org/10.1111/j.1460-9568.1993.tb00941.x CrossRefPubMed

Schmidt KC, Smith CB (2005) Resolution, sensitivity and precision with autoradiography and small animal positron emission tomography: implications for functional brain imaging in animal research. Nucl Med Biol 32:719–725. https://doi.org/10.1016/j.nucmedbio.2005.04.020 CrossRefPubMed

Schmiedt RA, Mills JH, Boettcher FA (1996) Age-related loss of activity of auditory-nerve fibers. J Neurophysiol 76:2799–2803CrossRef

Schwender D, Rimkus T, Haessler R, Klasing S, Poppel E, Peter K (1993) Effects of increasing doses of alfentanil, fentanyl and morphine on mid-latency auditory evoked potentials. Br J Anaesth 71:622–628CrossRef

Shamma S, Fritz J (2014) Adaptive auditory computations. Curr Opin Neurobiol 25:164–168. https://doi.org/10.1016/j.conb.2014.01.011 CrossRefPubMedPubMedCentral

Sharp FR, Ryan AF, Goodwin P, Woolf NK (1981) Increasing intensities of wide band noise increase [14C]2-deoxyglucose uptake in gerbil central auditory structures. Brain Res 230(1–2):87–96CrossRef

Siikanen J, Sjövall J, Forslid A, Brun E, Bjurberg M, Wennerberg J, Ekblad L, Sandell A (2015) An anesthetic method compatible with ¹⁸F-FDG-PET studies in mice. Am J Nucl Med Mol Imaging 5:270–277PubMedPubMedCentral

Sinnott JM, Mosqueda SB (2003) Effects of aging on speech sound discrimination in the Mongolian gerbil. Ear Hear 24:30–37. https://doi.org/10.1097/01.aud.0000051747.58107.89 CrossRefPubMed

Toyama H, Ichise M, Liow J-S, Vines DC, Seneca NM, Modell KJ, Seidel J, Green MV, Innis RB (2004) Evaluation of anesthesia effects on [¹⁸F]FDG uptake in mouse brain and heart using small animal PET. Nucl Med Biol 31:251–256. https://doi.org/10.1016/S0969-8051(03)00124-0 CrossRefPubMed

Tucci DL, Cant NB, Durham D (1999) Conductive hearing loss results in a decrease in central auditory system activity in the young gerbil. Laryngoscope 109(9):1359–1371. https://doi.org/10.1097/00005537-199909000-00001 CrossRefPubMed

Walker KMM, Bizley JK, King AJ, Schnupp JWH (2011) Multiplexed and robust representations of sound features in auditory cortex. J Neurosci 31:14565CrossRef

Wang ZX, Ryan AF, Woolf NK (1987) Pentobarbital and ketamine alter the pattern of 2-deoxyglucose uptake in the central auditory system of the gerbil. Hearing Res 27(2):145–155CrossRef

Willmore BDB, King AJ (2009) Auditory cortex: representation through Sparsification? Cur Biol 19:R1123–R1125. https://doi.org/10.1016/j.cub.2009.11.003 CrossRef

Yu X, Wadghiri YZ, Sanes DH, Turnbull DH (2005) In vivo auditory brain mapping in mice with Mn-enhanced MRI. Nat Neurosci 8:961–968. https://doi.org/10.1038/nn1477 CrossRefPubMedPubMedCentral

Titel: Activation in the auditory pathway of the gerbil studied with 18F-FDG PET: effects of anesthesia
verfasst von: M. Kessler
M. Mamach
R. Beutelmann
J. P. Bankstahl
F. M. Bengel
G. M. Klump
Georg Berding
Publikationsdatum: 10.09.2018
Verlag: Springer Berlin Heidelberg
Erschienen in: Brain Structure and Function / Ausgabe 9/2018
Print ISSN: 1863-2653
Elektronische ISSN: 1863-2661
DOI: https://doi.org/10.1007/s00429-018-1743-9

Leitlinien kompakt für die Neurologie

Mit medbee Pocketcards sicher entscheiden.

^{Seit 2022 gehört die medbee GmbH zum Springer Medizin Verlag}

Kostenlos registrieren

Neu im Fachgebiet Neurologie

23.04.2024 | Parkinson-Krankheit | Podcast | Nachrichten

Update Neurologie

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.

Newsletter bestellen

Live-Webinar: Aktuelle Leitlinien bei Herz-Kreislauf-Erkrankungen

Springer Medizin

Activation in the auditory pathway of the gerbil studied with ¹⁸F-FDG PET: effects of anesthesia

Abstract

Leitlinien kompakt für die Neurologie

Neu im Fachgebiet Neurologie

Parkinson-Therapie im Wandel – aktuelle Leitlinie im Fokus

Auf diese Krankheiten bei Geflüchteten sollten Sie vorbereitet sein

Hustenstiller lindert Agitation bei Alzheimer

Checkpointhemmer auch bei MS sicher

Update Neurologie

Live-Webinar: Aktuelle Leitlinien bei Herz-Kreislauf-Erkrankungen

Springer Medizin

Abstract

Bitte loggen Sie sich ein, um Zugang zu diesem Inhalt zu erhalten

Weitere Artikel der Ausgabe 9/2018

Hippocampal proBDNF facilitates place learning strategy associated with neural activity in rats

Claustrum circuit components for top–down input processing and cortical broadcast

A characterization of laminar architecture in mouse primary auditory cortex

Development of piriform cortex interhemispheric connections via the anterior commissure: progressive and regressive strategies

Immediate early gene expression related to learning and retention of a visual discrimination task in bamboo sharks (Chiloscyllium griseum)

Development of the P300 from childhood to adulthood: a multimodal EEG and MRI study

Leitlinien kompakt für die Neurologie

Neu im Fachgebiet Neurologie

Parkinson-Therapie im Wandel – aktuelle Leitlinie im Fokus

Auf diese Krankheiten bei Geflüchteten sollten Sie vorbereitet sein

Hustenstiller lindert Agitation bei Alzheimer

Checkpointhemmer auch bei MS sicher

Update Neurologie