Auditory functional magnetic resonance imaging in dogs – normalization and group analysis and the processing of pitch in the canine auditory pathways
Tóm tắt
Functional magnetic resonance imaging (fMRI) is an advanced and frequently used technique for studying brain functions in humans and increasingly so in animals. A key element of analyzing fMRI data is group analysis, for which valid spatial normalization is a prerequisite. In the current study we applied normalization and group analysis to a dataset from an auditory functional MRI experiment in anesthetized beagles. The stimulation paradigm used in the experiment was composed of simple Gaussian noise and regular interval sounds (RIS), which included a periodicity pitch as an additional sound feature. The results from the performed group analysis were compared with those from single animal analysis. In addition to this, the data were examined for brain regions showing an increased activation associated with the perception of pitch. With the group analysis, significant activations matching the position of the right superior olivary nucleus, lateral lemniscus and internal capsule were identified, which could not be detected in the single animal analysis. In addition, a large cluster of activated voxels in the auditory cortex was found. The contrast of the RIS condition (including pitch) with Gaussian noise (no pitch) showed a significant effect in a region matching the location of the left medial geniculate nucleus. By using group analysis additional activated areas along the canine auditory pathways could be identified in comparison to single animal analysis. It was possible to demonstrate a pitch-specific effect, indicating that group analysis is a suitable method for improving the results of auditory fMRI studies in dogs and extending our knowledge of canine neuroanatomy.
Tài liệu tham khảo
Strain GM. Canine deafness. Vet Clin North Am Small Anim Pract. 2012;42(6):1209–24.
McBrearty A, Penderis J. Transient evoked otoacoustic emissions testing for screening of sensorineural deafness in puppies. J Vet Intern Med. 2011;25(6):1366–71.
Penrod JP, Coulter DB. The diagnostic uses of impedance audiometry in the dog. J Am Anim Hosp Assoc. 1980;16:941–8.
Scheifele PM, Clark JG. Electrodiagnostic evaluation of auditory function in the dog. Vet Clin North Am Small Anim Pract. 2012;42(6):1241–57.
Sockalingam R, Filippich L, Sommerlad S, Murdoch B, Charles B. Transient-evoked and 2 F1-F2 distortion product oto-acoustic emissions in dogs: preliminary findings. Audiol Neurootol. 1998;3(6):373–85.
Strain GM. Congenital deafness and its recognition. Vet Clin North Am Small Anim Pract. 1999;29(4):895–907. vi.
Webb AA. Brainstem auditory evoked response (BAER) testing in animals. Can Vet J. 2009;50(3):313–8.
Wilson WJ, Mills PC. Brainstem auditory-evoked response in dogs. Am J Vet Res. 2005;66(12):2177–87.
Strain GM. Brainstem Auditory Evoked Response (BAER). In: Deafness in Dogs and Cats. Cambridge: CABI; 2011.
Merzenich MM, Knight PL, Roth GL. Representation of cochlea within primary auditory cortex in the cat. J Neurophysiol. 1975;38(2):231–49.
Hall DA. fMRI of the Auditory Cortex. In: Faro SH, editor. Functional MRI: basic principles and clinical applications. New York: Springer; 2006.
Villringer A, Dirnagl U. Coupling of brain activity and cerebral blood flow: basis of functional neuroimaging. Cerebrovasc Brain Metab Rev. 1995;7(3):240–76.
Binder JR, Rao SM, Hammeke TA, Yetkin FZ, Jesmanowicz A, Bandettini PA, Wong EC, Estkowski LD, Goldstein MD, Haughton VM, et al. Functional magnetic resonance imaging of human auditory cortex. Ann Neurol. 1994;35(6):662–72.
Kovacs S, Peeters R, Smits M, De Ridder D, Van Hecke P, Sunaert S. Activation of cortical and subcortical auditory structures at 3 T by means of a functional magnetic resonance imaging paradigm suitable for clinical use. Invest Radiol. 2006;41(2):87–96.
Talavage TM, Gonzalez-Castillo J, Scott SK. Auditory neuroimaging with fMRI and PET. Hear Res. 2014;307:4–15.
Patterson RD, Uppenkamp S, Johnsrude IS, Griffiths TD. The processing of temporal pitch and melody information in auditory cortex. Neuron. 2002;36(4):767–76.
Plack CJ, Barker D, Hall DA. Pitch coding and pitch processing in the human brain. Hear Res. 2014;307:53–64
Cheung MM, Lau C, Zhou IY, Chan KC, Cheng JS, Zhang JW, Ho LC, Wu EX. BOLD fMRI investigation of the rat auditory pathway and tonotopic organization. Neuroimage. 2012;60(2):1205–11.
Voss HU, Salgado-Commissariat D, Helekar SA. Altered auditory BOLD response to conspecific birdsong in zebra finches with stuttered syllables. PLoS One. 2010;5(12):e14415.
Aguirre GK, Komaromy AM, Cideciyan AV, Brainard DH, Aleman TS, Roman AJ, Avants BB, Gee JC, Korczykowski M, Hauswirth WW, et al. Canine and human visual cortex intact and responsive despite early retinal blindness from RPE65 mutation. PLoS Med. 2007;4(6):e230.
Brown TA, Joanisse MF, Gati JS, Hughes SM, Nixon PL, Menon RS, Lomber SG. Characterization of the blood-oxygen level-dependent (BOLD) response in cat auditory cortex using high-field fMRI. Neuroimage. 2013;64:458–65.
Chen G, Wang F, Dillenburger BC, Friedman RM, Chen LM, Gore JC, Avison MJ, Roe AW. Functional magnetic resonance imaging of awake monkeys: some approaches for improving imaging quality. Magn Reson Imaging. 2012;30(1):36–47.
Stefanacci L, Reber P, Costanza J, Wong E, Buxton R, Zola S, Squire L, Albright T. fMRI of monkey visual cortex. Neuron. 1998;20(6):1051–7.
Willis CK, Quinn RP, McDonell WM, Gati J, Parent J, Nicolle D. Functional MRI as a tool to assess vision in dogs: the optimal anesthetic. Vet Ophthalmol. 2001;4(4):243–53.
Petkov CI, Kayser C, Augath M, Logothetis NK. Optimizing the imaging of the monkey auditory cortex: sparse vs. continuous fMRI. Magn Reson Imaging. 2009;27(8):1065–73.
Lahti KM, Ferris CF, Li F, Sotak CH, King JA. Comparison of evoked cortical activity in conscious and propofol-anesthetized rats using functional MRI. Magn Reson Med. 1999;41(2):412–6.
Huettel SA, Song AW, McCarthy G. Functional magnetic resonance imaging, vol. 1: Sinauer Associates Sunderland, MA; 2004.
Ashburner J, Friston K. Multimodal image coregistration and partitioning--a unified framework. Neuroimage. 1997;6(3):209–17.
Brett M, Johnsrude IS, Owen AM. The problem of functional localization in the human brain. Nat Rev Neurosci. 2002;3(3):243–9.
Crinion J, Ashburner J, Leff A, Brett M, Price C, Friston K. Spatial normalization of lesioned brains: performance evaluation and impact on fMRI analyses. Neuroimage. 2007;37(3):866–75.
Jiang D, Du Y, Cheng H, Jiang T, Fan Y. Groupwise spatial normalization of fMRI data based on multi-range functional connectivity patterns. Neuroimage. 2013;82:355–72.
Yost WA. Pitch of iterated rippled noise. J Acoust Soc Am. 1996;100(1):511–8.
Bach JP, Lupke M, Dziallas P, Wefstaedt P, Uppenkamp S, Seifert H, Nolte I. Functional magnetic resonance imaging of the ascending stages of the auditory system in dogs. BMC Vet Res. 2013;9:210.
Datta R, Lee J, Duda J, Avants BB, Vite CH, Tseng B, Gee JC, Aguirre GD, Aguirre GK. A digital atlas of the dog brain. PLoS One. 2012;7(12):e52140.
Hall DA, Haggard MP, Akeroyd MA, Palmer AR, Summerfield AQ, Elliott MR, Gurney EM, Bowtell RW. “Sparse” temporal sampling in auditory fMRI. Hum Brain Mapp. 1999;7(3):213–23.
Brazis P, Masdeu J, Biller J. Localization in Clinical Neurology. Alphen aan den Rijn, Netherlands: Wolters Kluwer; 2011.
Goldberg JM, Brown PB. Functional organization of the dog superior olivary complex: an anatomical and electrophysiological study. J Neurophysiol. 1968;31(4):639–56.
Heffner H. Effect of auditory cortex ablation on localization and discrimination of brief sounds. J Neurophysiol. 1978;41(4):963–76.
Stepień I, Stepień L, Lubińska E. Function of dog’s auditory cortex in tests involving auditory location cues and directional instrumental response. Acta Neurobiol Exp. 1989;50(1-2):1–12.
Andics A, Gacsi M, Farago T, Kis A, Miklosi A. Voice-sensitive regions in the dog and human brain are revealed by comparative fMRI. Curr Biol. 2014;24(5):574–8.
Hall AJ, Brown TA, Grahn JA, Gati JS, Nixon PL, Hughes SM, Menon RS, Lomber SG. There’s more than one way to scan a cat: imaging cat auditory cortex with high-field fMRI using continuous or sparse sampling. J Neurosci Methods. 2014;224:96–106.
Singer M. The Brain of the Dog in Section. W. B. Saunders Company, 1962. Plates 19-49, 62-88, 97-124.
Griffiths TD, Uppenkamp S, Johnsrude I, Josephs O, Patterson RD. Encoding of the temporal regularity of sound in the human brainstem. Nat Neurosci. 2001;4(6):633–7.
Walker KM, Bizley JK, King AJ, Schnupp JW. Cortical encoding of pitch: recent results and open questions. Hear Res. 2011;271(1-2):74–87.
Gelfer MP, Mikos VA. The relative contributions of speaking fundamental frequency and formant frequencies to gender identification based on isolated vowels. J Voice. 2005;19(4):544–54.
Smith DR, Patterson RD, Turner R, Kawahara H, Irino T. The processing and perception of size information in speech sounds. J Acoust Soc Am. 2005;117(1):305–18.
Capranica RR. Vocal response of the bullfrog to natural and synthetic mating calls. J Acoust Soc Am. 1966;40(5):1131–9.
Koda H, Masataka N. A pattern of common acoustic modification by human mothers to gain attention of a child and by macaques of others in their group. Psychol Rep. 2002;91(2):421–2.
Kojima S, Izumi A, Ceugniet M. Identification of vocalizers by pant hoots, pant grunts and screams in a chimpanzee. Primates. 2003;44(3):225–30.
Nelson DA. Song frequency as a cue for recognition of species and individuals in the field sparrow (Spizella pusilla). J Comp Psychol. 1989;103(2):171.
Berns GS, Brooks AM, Spivak M. Functional MRI in awake unrestrained dogs. PLoS One. 2012;7(5):e38027.
Berns GS, Brooks AM, Spivak M. Scent of the familiar: An fMRI study of canine brain responses to familiar and unfamiliar human and dog odors. Behav Processes. 2014; 110: 37-46.
Peelle JE, Eason RJ, Schmitter S, Schwarzbauer C, Davis MH. Evaluating an acoustically quiet EPI sequence for use in fMRI studies of speech and auditory processing. Neuroimage. 2010;52(4):1410–9.
Brett M, Valbregue R, Poline J-B. Region of interest analysis using the MarsBar toolbox for SPM 99. NeuroImage. 2002; 16:497.
Palazzi X. The Beagle Brain in Stereotaxic Coordinates.New York, USA: Springer Science + Business Media; 2011. pp 67-77, 89-95.