Elsevier

NeuroImage

Volume 65, 15 January 2013, Pages 119-126
NeuroImage

Functional magnetic resonance imaging of sound pressure level encoding in the rat central auditory system

https://doi.org/10.1016/j.neuroimage.2012.09.069Get rights and content

Abstract

Intensity is an important physical property of a sound wave and is customarily reported as sound pressure level (SPL). Invasive techniques such as electrical recordings, which typically examine one brain region at a time, have been used to study neuronal encoding of SPL throughout the central auditory system. Non-invasive functional magnetic resonance imaging (fMRI) with large field of view can simultaneously examine multiple auditory structures. We applied fMRI to measure the hemodynamic responses in the rat brain during sound stimulation at seven SPLs over a 72 dB range. This study used a sparse temporal sampling paradigm to reduce the adverse effects of scanner noise. Hemodynamic responses were measured from the central nucleus of the inferior colliculus (CIC), external cortex of the inferior colliculus (ECIC), lateral lemniscus (LL), medial geniculate body (MGB), and auditory cortex (AC). BOLD signal changes generally increase significantly (p < 0.001) with SPL and the dependence is monotonic in CIC, ECIC, and LL. The ECIC has higher BOLD signal change than CIC and LL at high SPLs. The difference between BOLD signal changes at high and low SPLs is less in the MGB and AC. This suggests that the SPL dependences of the LL and IC are different from those in the MGB and AC and the SPL dependence of the CIC is different from that of the ECIC. These observations are likely related to earlier observations that neurons with firing rates that increase monotonically with SPL are dominant in the CIC, ECIC, and LL while non-monotonic neurons are dominant in the MGB and AC. Further, the IC's SPL dependence measured in this study is very similar to that measured in our earlier study using the continuous imaging method. Therefore, sparse temporal sampling may not be a prerequisite in auditory fMRI studies of the IC.

Introduction

Hearing is a complex ability that converts information from the sound pressure wave into perceptions. Vibrations of the sound wave cause displacements of the basilar membrane and the organ of Corti moves with the basilar membrane. The electrical signals are transduced from mechanical vibrations by the organ of Corti and transferred to the cochlear nucleus (CN) (Dallos and Corey, 1991). The CN sends the signals to the ipsilateral and contralateral superior olivary complexes (SOCs). Signals are then primarily transferred to the contralateral lateral lemniscus (LL), inferior colliculus (IC), medial geniculate body (MGB) and primary auditory cortex (AC) (Longstaff, 2005). The IC is composed of a central nucleus (CIC) adjacent to the external cortical nucleus (ECIC) (Winer and Schreiner, 2005). These structures are responsible for processing the physical information of the sound. One important piece of information is intensity, which is customarily reported as sound pressure level (SPL) (Pierce, 1989). Intensity is important for mediating arousal, emotions, and motivations (Bradley and Lang, 2000) and it is frequently studied in auditory neuroscience. For adult humans, intensity is one of the key stimulus features used to estimate target distance (Barbour, 2011).

Auditory neuroscience has primarily used psychophysical and invasive techniques to study SPL encoding in the brain. Psychophysical techniques have been used extensively to study how SPL and other sound properties, such as the critical bandwidth (Zwicker et al., 1957) and duration (Florentine et al., 1996), affect the perception of loudness (Fletcher and Munson, 1933, Moore et al., 1997, Zwicker and Scharf, 1965). Invasive electrical recording studies have reported SPL dependence in neuronal firing rates throughout the brain (Barone et al., 1996, Kelly et al., 1998, Palombi and Caspary, 1996b, Polley et al., 2007, Semple and Kitzes, 1993, Tan et al., 2007, Wu et al., 2006, Zhang et al., 2004, Zhang et al., 2006). Minimally invasive optical imaging has also been used to examine the auditory cortex (Higgins et al., 2010, Kalatsky et al., 2005, Storace et al., 2010). In contrast to traditional invasive techniques, non-invasive functional magnetic resonance imaging (fMRI) has large field of view and can simultaneously examine multiple auditory structures (Cheung et al., 2012a, Jancke et al., 1998, Sigalovsky and Melcher, 2006). Blood oxygenation level-dependent (BOLD) contrast measures the hemodynamic response and is the most widely used contrast in fMRI (Ogawa et al., 1990). Measuring changes in the hemodynamic response with SPL provides a means to examine SPL encoding in the auditory system.

The majority of fMRI studies are performed using the conventional continuous imaging method, where image acquisition is equally spaced during the repetition time (TR) (Brechmann et al., 2002, Cheung et al., 2012a, Cheung et al., 2012b, Jancke et al., 1998, Mohr et al., 1999, Sigalovsky and Melcher, 2006, Talavage and Hall, 2012). Continuous imaging is potentially problematic for fMRI investigations of auditory physiology because the acoustic scanner noise is present during auditory stimulus presentation (Moelker and Pattynama, 2003). A sparse temporal sampling paradigm can reduce the adverse effects of scanner noise (Hall et al., 1999). In sparse imaging, a single image volume is acquired shortly after the end of stimulus and baseline conditions. Functional imaging is still possible because the hemodynamic delay causes the fMRI signal change to occur several seconds after the stimulus. Importantly, the sound stimulus is not corrupted by the scanner noise as long as TR is considerably longer than the duration of the hemodynamic response (Hall et al., 1999). Most human auditory fMRI studies, using continuous or sparse imaging, have only examined the cortex, although some studies have examined subcortical structures (Abrams et al., 2011, Griffiths et al., 2001, Guimaraes et al., 1998, Kovacs et al., 2006, Krumbholz et al., 2005, Melcher et al., 2000, Röhl and Uppenkamp, 2012, Röhl et al., 2011, Schönwiesner et al., 2007, Sigalovsky and Melcher, 2006, Thompson et al., 2006). Subcortical structures, such as the IC, have been studied less partly because of their small size, motion related to cardiac pulsations, severe susceptibility artifacts (Di Salle et al., 2003), and deep position near the brainstem. The rat is a suitable model for functional imaging studies of the subcortex because its subcortex occupies a larger portion of the brain and is located closer to the skull compared to in humans (Glendenning and Masterton, 1998). The rat's hearing is also much more sensitive than that of a human at high frequencies. Humans can hear a 10 dB SPL sound with frequency from 250 Hz to 8.1 kHz while a rat can hear the sound from 5 to 45 kHz (Heffner and Heffner, 2007).

In this study, we apply fMRI with sparse temporal sampling to measure the hemodynamic responses in the rat CIC, ECIC, LL, MGB, and AC during auditory stimulation at seven SPLs over a 72 dB range. fMRI is well suited to measuring, analyzing, and comparing the SPL effect on different structures at the same time. This study represents the first application of sparse temporal sampling in rat auditory fMRI.

Section snippets

Animal preparation

All aspects of this study were approved by the local animal ethics committee. Animals were prepared for fMRI sessions as described in our earlier studies (Chan et al., 2011, Cheung et al., 2012a, Cheung et al., 2012b, Lau et al., 2011a, Lau et al., 2011b, Zhou et al., 2011). Normal male Sprague–Dawley rats (200–250 g, N = 7) were used in this study. Rats were anesthetized with 3% isofluorane for induction and maintained at 1% throughout the course of scanning. The rat was placed in the prone

Results

Fig. 2 shows the 89 dB broadband noise spectrum used for the experiment. The main frequency component is 1 to 40 kHz and the total SPL is obtained by summation of the mean square sound pressures of all frequencies. The other six stimuli used in the experiment have the same spectral shape but vary in SPL.

Fig. 3A shows the t-value map from a representative animal computed from the fMRI images stimulated by the noise shown in Fig. 2. Refer to Supplementary Fig. 1A to see the map overlaid on an

Discussion

This study applied BOLD fMRI to measure the hemodynamic response in the rat brain under seven different auditory stimulation SPL settings. Significant BOLD signal changes are observed in the CIC, ECIC, LL, MGB, and AC. BOLD signal changes generally increase significantly with SPL in CIC, ECIC, and LL. The difference between BOLD signal changes at high and low SPLs is less in the MGB and AC. The ECIC has significantly higher BOLD signal changes than the CIC and LL at high SPLs. This suggests

Conclusion

This study applied BOLD fMRI to measure the hemodynamic responses in the rat auditory system to sound stimulation over a broad range of SPLs using sparse temporal sampling. In the CIC, ECIC, and LL, BOLD signal changes generally increase significantly with SPL and the ECIC has significantly higher response than the CIC and LL at high SPLs. In the MGB and AC, the increases of BOLD signal changes from low to high SPLs are less. This suggests that the SPL dependences of the LL and IC are different

Acknowledgments

This work was supported in part by Hong Kong Research Grants Council (HKU7837/11M).

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    Authors Jevin W. Zhang and Condon Lau contributed equally to this study.

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