High resolution functional imaging of the auditory pathway and cortex

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1 High resolution functional imaging of the auditory pathway and cortex Elia Formisano Maastricht-Brain Imaging Center (M-BIC) Faculty of Psychology and Neuroscience Maastricht University, The Netherlands

2

3 7 Tesla Functional MRI Temporal lobe The location of the primary auditory cortex in the human brain (Heschl s gyrus) Formisano et al., Neuron, 2003 (1.5 x 1. 5x 1.5 mm 3 )

4 Mapping tonotopy with fmri Heschl s gyrus Active brain region

5 5 Formisano et al. (2003), Moerel et al. (2012), De Martino et al(2014), De Martino et al (2015)

6 Can we image the detailed tonotopy of sub-cortical auditory nuclei in humans? Very small structures (e.g. human IC ~ 120 mm 3 ; human MGB ~ 100 mm 3 ) High resolution fmri (<= 1.5 mm 7T)

7 dorso-lateral (low) to ventro-medial (high) gradient Tonotopic mapping (7T) in human Inferior Colliculus De Martino et al.. (Nature Communications, 2013)

8 Frequency tuning-width representation in the human IC. Best Frequency De Martino et al., (2013)

9 ...in comparison to the cortex. De Martino et al., (2013)

10 Tonotopic maps in human MGB Moerel et al.,scientific Reports, 2015

11 Tonotopic maps in human MGB superior posterior Frequency right left Low High anterior inferior At superior locations: Low to high gradient from medial to lateral locations Moving inferior: Additional gradient, resulting in low-high-low tonotopic map Moerel et al. (2015)

12 sit1 based alignment Talairach Improving inter subject correspondence using anatomical contrast Coronal LGN Transversal MGB Tourdias et al. (2014) Moerel et al. (2015)

13 Tonotopic responses in unilateral tinnitus Tinnitus Controls COR SAG COR SAG Right Left (Contralateral To Tinnitus) Right Frequency Right Left Right Low High Eva Berlot (OHBM2016, Poster no. 2284)

14 Faruk Gülban (OHBM2016, Poster no. 1692)

15 Faruk Gülban (OHBM2016, Poster no. 1692)

16 Thalamo-cortical connections MGB SO F-value (response to natural sounds) Probabilistic Connections MGB Planum Temporale Low High Low High

17 frequency Auditory processing across layers in primary auditory cortex ~ 3-4 mm PT PAC H G PAC granular to other areas Post mortem anatomy frequency from other areas thalamus

18 Sub-millimeter functional MRI (7 & 9.4 Tesla) Auditory cortex response to FM tones Post mortem anatomy In vivo 7T fmri (GRASE): 0.8 x 0.8 x 0.8 mm 3 FM sweeps Auditory task (FM sweep direction) Visual task (change detection) De Martino et al., PNAS (2015) In collaboration with: Essa Yacoub, Kamil Ugurbil (CMRR)

19 De Martino et al., PNAS, (2015)

20 Tonotopic maps in human AC at sub-millimeter resolution (cortical surface maps) Medial Lateral High (6400) Frequency (Hz) Post mortem anatomy Low (200) Posterior Anterior

21 Tonotopic maps in human AC at sub-millimeter resolution (volume rendering) Medial High (6400) Frequency (Hz) Cortical Ribbon Low (200) Lateral

22 Cortical depth sampling of the Heschl s Gyrus (video)

23 Cortical depth sampling of the Heschl s Gyrus

24 HG Lateral Myelin-related contrast (T1/T2*) Anterior Medial Posterior WM CSF

25 Tonotopic maps (GRASE) Auditory Task (FM direction) Visual Task WM CSF

26 Detecting columnar organization. Low Freq. High Freq. f y f z f x f z 2 << f x2 +f y 2 Tonotopic Map Tonotopic Map Gradient Single Grid Point Gradient Column

27 Columnar cortex in Heschl s gyrus De Martino et al, PNAS, (2015) Session 1 Session 2

28 Columnar primary auditory cortex (video) De Martino et al., PNAS, (2015)

29 Cortical depth dependent task modulations CSF WM De Martino et al., PNAS, (2015)

30 Cortical-depth analysis - Summary 3D-GRASE allowed measuring T 2 weighted functional responses in the HG with high isotropic resolution (0.8 mm iso). Low (200) Frequency (Hz) High (6400) The columnar arrangement of frequency preference could be imaged in portions of HG. Low Anatomical Contrast High These same locations were characterized with deep myelin related anatomical contrast, (in agreement with post mortem definition of area AI). In columnar regions, top-down effects of attention were most prominent in superficial layers. De Martino et al., PNAS, (2015)

31 Beyond frequency: Features of natural sounds modelbased analysis of fmri responses (encoding) VS Voxel receptive field models Santoro et al., 2015

32 Prediction Accuracy Imaging multi-features tuning across cortical depth Subject 2 - Left Subject 3 - Left Subject 5 - Left T 1 /T 2 * contrast high low Primary auditory cortex Non-primary auditory cortex Joint modulation model Independent modulation model Tonotopy model Cortical depth Cortical depth Joint feature tuning emerges in superficial depths of PAC Joint feature tuning better model throughout cortical depths in the non-primary auditory cortex Moerel et al.,(work in progress)

33 Audition and Methods Group Emily Allen (Minneapolis) Milene Bonte Xu Chen Vittoria De Angelis Kiki Derey Federico De Martino Niels Diesbergen Julia Erb Faruk Gülban Lars Hausfeld Valentin Kemper Michelle Moerel Lars Riecke Past members: Anke Ley (DFG), Noël Staeren, Hanna Renvall Nick Kilian-Hütten, Roberta Santoro Martha Shiell Fren Smulders Jessica Thompson (Montreal) Shruti Ullas Giancarlo Valente Thanks to Rainer Goebel Kamil Uludag, Anna Gardumi Essa Yacoub, Kamil Ugurbil, Gregor Adriany (coils), Scott Schillack (coils) Wim Vanduffel (monkey fmri)

34 References Formisano, E., Moerel, M., Bonte, M., Functional MRI of the human auditory cortex (2015). In: Functional MRI: From Nuclear Spins to Brain Function, K. Uludağ, K. Uğurbil, and L. J. Berliner (Eds.), Springer. De Martino F, Moerel M, Ugurbil K, Goebel R, Yacoub E, Formisano E. (2015) Frequency preference and attention effects across cortical depths in the human primary auditory cortex. Proc Natl Acad Sci U S A. Dec 29;112(52): doi: /pnas PubMed PMID: Moerel M, De Martino F, Uğurbil K, Yacoub E, Formisano E. (2015) Processing of frequency and location in human subcortical auditory structures. Sci Rep. Nov 24;5: doi: /srep PMID: ; PMCID: PMC Moerel M, De Martino F, Formisano E. (2014) An anatomical and functional topography of human auditory cortical areas. Front Neurosci Jul 29;8:225. doi: /fnins PMID: ; PMCID: PMC Santoro R, Moerel M, De Martino F, Goebel R, Ugurbil K, Yacoub E, Formisano E (2014) Encoding of Natural Sounds at Multiple Spectral and Temporal Resolutions in the Human Auditory Cortex. Plos Computational Biology. 10(1):e De Martino F, Moerel M, van de Moortele PF, Ugurbil K, Goebel R, Yacoub E, Formisano E. (2013) Spatial organization of frequency preference and selectivity in the human inferior colliculus. Nat Commun. 4:1386. doi: /ncomms2379. PMID: ; PMCID: PMC De Martino F, Moerel M, Xu J, van de Moortele PF, Ugurbil K, Goebel R, Yacoub E, Formisano E. (2014) High resolution mapping of myelo-architecture in vivo: localization of auditory areas in the human brain. Cerebral Cortex pii: bhu150. Moerel, M., De Martino, F., and Formisano, E. (2012). Processing of Natural Sounds in Human Auditory Cortex: tonotopy, spectral tuning and relation to voice-sensitivity. The Journal of Neuroscience Formisano, E., Kim, D. S., Di Salle, F., van de Moortele, P. F., Ugurbil, K., and Goebel, R. (2003). Mirrorsymmetric tonotopic maps in human primary auditory cortex. Neuron 40,

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