Elsevier

NeuroImage

Volume 91, 1 May 2014, Pages 220-227
NeuroImage

The inferior colliculus is involved in deviant sound detection as revealed by BOLD fMRI

https://doi.org/10.1016/j.neuroimage.2014.01.043Get rights and content

Highlights

  • BOLD fMRI was applied to investigate the role of the IC in deviance detection.

  • Deviant and standard had identical frequency spectra but inverted time profiles.

  • Potential confound from physical differences between the two sounds was ruled out.

  • The IC is involved in deviance detection.

  • BOLD fMRI revealed the highly adaptive nature of neurons in the medial IC.

Abstract

Rapid detection of deviant sounds is a crucial property of the auditory system because it increases the saliency of biologically important, unexpected sounds. The oddball paradigm in which a deviant sound is randomly interspersed among a train of standard sounds has been traditionally used to study this property in mammals. Currently, most human studies have only revealed the involvement of cortical regions in this property. Recently, several animal electrophysiological studies have reported that neurons in the inferior colliculus (IC) exhibit reduced responses to a standard sound but restore their responses at the occurrence of a deviant sound (i.e., stimulus-specific adaptation or SSA), suggesting that the IC may also be involved in deviance detection. However, by adopting an invasive method, these animal studies examined only a limited number of neurons. Although SSA appears to be more prominent in the external cortical nuclei of the IC for frequency deviant, a thorough investigation of this property throughout the IC using other deviants and efficient imaging techniques may provide more comprehensive information on this important phenomenon. In this study, blood-oxygen-level-dependent (BOLD) fMRI with a large field of view was applied to investigate the role of the IC in deviance detection. Two sound tokens that had identical frequency spectrum but temporally inverted profiles were used as the deviant and standard. A control experiment showed that these two sounds evoked the same responses in the IC when they were separately presented. Two oddball experiments showed that the deviant induced higher responses than the standard (by 0.41 ± 0.09% and 0.41 ± 0.10%, respectively). The most activated voxels were in the medial side of the IC in both oddball experiments. The results clearly demonstrated that the IC is involved in deviance detection. BOLD fMRI detection of increased activities in the medial side of the IC to the deviant revealed the highly adaptive nature of a substantial population of neurons in this region, probably those that belong to the rostral or dorsal cortex of the IC. These findings highlighted the complexity of auditory information processing in the IC and may guide future studies of the functional organizations of this subcortical structure.

Introduction

Rapid detection of deviant sounds in complex environments is essential for an individual's survival. Auditory neuroscience has extensively studied the underlying mechanisms of deviance detection in the mammalian auditory system, usually by adopting an oddball paradigm in which a rare sound (the deviant) is randomly interspersed with low occurrence probability in a train of repetitive sounds (the standard). In humans, the deviant sounds can evoke a negative deflection in the auditory event-related potentials, the mismatch negativity (MMN) (Kujala et al., 2007, Naatanen et al., 2007). Multiple studies have investigated the neural correlates of the MMN waveform and suggested that deviance detection is a function of mainly cortical regions, such as the superior temporal gyrus, the Heschl's gyrus and the inferior frontal gyrus (Doeller et al., 2003, Giard et al., 1995, Liebenthal et al., 2003, Molholm et al., 2005, Muller et al., 2002, Opitz et al., 1999, Opitz et al., 2002, Rosburg et al., 2005, Sabri et al., 2004, Schonwiesner et al., 2007).

Recently, several animal electrophysiological studies have reported that neurons at both cortical and subcortical levels share a property called stimulus-specific adaptation (SSA). SSA refers to a phenomenon in which a neuron exhibits reduced responses to a repetitive sound, but restores the responses at the occurrence of a deviant sound. This phenomenon has been observed not only in the auditory cortex (Ulanovsky et al., 2003, Ulanovsky et al., 2004), but also in the medial geniculate body (Anderson et al., 2009, Antunes et al., 2010, Duque et al., in press) and the inferior colliculus (IC) (Malmierca et al., 2009, Perez-Gonzalez et al., 2005). In the auditory pathway, the IC is a subcortical relay center for all ascending projections to the medial geniculate body and cortex, thus a key station for auditory information processing (Winer and Schreiner, 2005). It is composed of a central nucleus (CNIC) that is surrounded rostrally by the rostral cortex (RCIC), laterally by the lateral cortex (LCIC) and dorsally by the dorsal cortex (DCIC) (Loftus et al., 2008, Malmierca et al., 2011). The finding of SSA in IC neurons indicates that the IC may also play a role in the detection of deviant sound (Ayala and Malmierca, 2013, Ayala et al., 2013, Malmierca et al., 2009).

However, adopting an invasive method, these animal studies examined only a limited number of neurons (Malmierca et al., 2009, Perez-Gonzalez et al., 2005). Although SSA was found to be more prominent in the RCIC, LCIC and DCIC for frequency deviant (Duque et al., 2012), a thorough investigation of SSA throughout the IC using other types of deviant and efficient imaging method may provide more comprehensive information on its role in deviance detection.

Functional magnetic resonance imaging (fMRI) is a non-invasive technique that can cover a large field of view and can be used to measure the hemodynamic responses as neural correlates (Logothetis et al., 2001) in multiple brain structures with relatively high spatial and temporal resolution. Since its introduction, fMRI based on the blood-oxygen-level-dependent (BOLD) contrast has been widely used in mapping brain functions for different types of sensory stimulation (Ogawa et al., 1990). For the auditory system, BOLD fMRI studies have been conducted to investigate auditory information processing (Barton et al., 2012, De Martino et al., 2013, Sigalovsky and Melcher, 2006). A number of studies have applied BOLD fMRI in humans to locate the cortical neural sources of the MMN waveform (Doeller et al., 2003, Liebenthal et al., 2003, Molholm et al., 2005, Opitz et al., 1999, Opitz et al., 2002, Sabri et al., 2004, Schonwiesner et al., 2007). Only a few animal auditory fMRI studies have been reported so far (Baumann et al., 2011, Boumans et al., 2007, Cheung et al., 2012a, Cheung et al., 2012b, Kayser et al., 2007, Lau et al., 2013, Tanji et al., 2010, Van Meir et al., 2005, Voss et al., 2007, Yu et al., 2005, Yu et al., 2007, Yu et al., 2008, Zhang et al., 2013). The results from these studies have demonstrated that auditory fMRI on animals can provide valuable insights into hearing mechanisms, especially in subcortical structures such as the IC (Cheung et al., 2012a, Cheung et al., 2012b, Zhang et al., 2013).

In this study, BOLD fMRI was applied to investigate the role of the IC in deviance detection, using the oddball paradigm for auditory stimulation. Two sound tokens that had identical frequency spectrum but temporally inverted profiles were used as the deviant and standard. The hypothesis was that the deviant would induce a higher BOLD signal than the standard. To rule out a potential confounding issue that higher BOLD signal could result from the physical difference between the deviant and standard, BOLD responses to the two sound tokens were compared in a control experiment and two oddball experiments with alternated deviant and standard were performed. With these measurements, the BOLD signal change evoked by the deviant in the IC was confirmed to stem from its low occurrence probability.

Section snippets

Animal preparation

All animal experiments were approved by the local animal research ethics committee. Animals were prepared for fMRI sessions as described in our previous studies (Chan et al., 2010, Cheung et al., 2012a, Cheung et al., 2012b, Lau et al., 2011, Lau et al., 2013, Zhang et al., 2013, Zhou et al., 2012). Briefly, normal male Sprague–Dawley rats (200–250 g, N = 22) were used in this study. They were initially anesthetized with 3% isoflurane and then mechanically ventilated via oral intubation. Then they

Results

Fig. 4a shows the activation (t-value) maps of Sound A and Sound B computed from the fMRI images of the six animals studied in the control experiment. The average across the six animals is shown in Fig. 4b. The left IC (contralateral to the side of stimulation) was activated robustly by both Sound A and Sound B. The number of activated voxels and their t-value maps were highly similar. More quantitatively, the same 30 voxels were observed to be activated in two average activation maps, and the

Discussion

The results of the present study showed that the BOLD responses in the IC to Sound A and Sound B were affected by their occurrence probabilities. When the sounds were presented separately in the control experiment, BOLD responses were the same as demonstrated by their consistent spatial and temporal patterns. On the other hand, when they were presented with different probabilities as deviant and standard in the oddball experiments, BOLD responses to the deviant were significantly higher than

Conclusions

The present fMRI study demonstrated that the subcortical IC is involved in deviance detection. The results revealed the highly adaptive nature of a substantial population of neurons in the activated voxels, probably those that are from the RCIC and DCIC. The increased activities in these neurons at the occurrence of a deviant sound were reported for the first time in a large spatial scale with BOLD fMRI. These findings highlighted the complexity of auditory information processing in the IC and

Acknowledgments

The authors thank Professor Dan H. Sanes from New York University for his insightful comments on the manuscript. They also thank Mr. Russell W. Chan and Mr. Leon C. Ho for their assistance in animal experiments and Dr. Shujuan Fan and Ms. Samantha J. Ma for their comments on the manuscript. This work was supported in part by the Hong Kong Research Grants Council (HKU7837/11M) and the Croucher Foundation.

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