To date it remains largely unknown how fundamental aspects of natural sounds, such as their spectral content and location in space, are processed in human subcortical structures. Here we exploited ...the high sensitivity and specificity of high field fMRI (7 Tesla) to examine the human inferior colliculus (IC) and medial geniculate body (MGB). Subcortical responses to natural sounds were well explained by an encoding model of sound processing that represented frequency and location jointly. Frequency tuning was organized in one tonotopic gradient in the IC, whereas two tonotopic maps characterized the MGB reflecting two MGB subdivisions. In contrast, no topographic pattern of preferred location was detected, beyond an overall preference for peripheral (as opposed to central) and contralateral locations. Our findings suggest the functional organization of frequency and location processing in human subcortical auditory structures, and pave the way for studying the subcortical to cortical interaction required to create coherent auditory percepts.
Neural processing of sounds in the dorsal and ventral streams of the (human) auditory cortex is optimized for analyzing fine-grained temporal and spectral information, respectively. Here we use a ...Wilson and Cowan firing-rate modeling framework to simulate spectro-temporal processing of sounds in these auditory streams and to investigate the link between neural population activity and behavioral results of psychoacoustic experiments. The proposed model consisted of two
(A1 and R, representing primary areas) and two
(
and
, representing rostral and caudal processing respectively) areas, differing in terms of their spectral and temporal response properties. First, we simulated the responses to amplitude modulated (AM) noise and tones. In agreement with electrophysiological results, we observed an area-dependent transition from a temporal (synchronization) to a rate code when moving from low to high modulation rates. Simulated neural responses in a task of amplitude modulation detection suggested that thresholds derived from population responses in
areas closely resembled those of psychoacoustic experiments in human listeners. For tones, simulated modulation threshold functions were found to be dependent on the carrier frequency. Second, we simulated the responses to complex tones with missing fundamental stimuli and found that synchronization of responses in the
area accurately encoded pitch, with the strength of synchronization depending on number and order of harmonic components. Finally, using speech stimuli, we showed that the spectral and temporal structure of the speech was reflected in parallel by the modeled areas. The analyses highlighted that the
stream coded with high spectral precision the aspects of the speech signal characterized by slow temporal changes (e.g., prosody), while the
stream encoded primarily the faster changes (e.g., phonemes, consonants, temporal pitch). Interestingly, the pitch of a speaker was encoded both spatially (i.e., tonotopically) in
area and temporally in
area. Overall, performed simulations showed that the model is valuable for generating hypotheses on how the different cortical areas/streams may contribute toward behaviorally relevant aspects of auditory processing. The model can be used in combination with physiological models of neurovascular coupling to generate predictions for human functional MRI experiments.
The precise delineation of auditory areas in vivo remains problematic. Histological analysis of postmortem tissue indicates that the relation of areal borders to macroanatomical landmarks is variable ...across subjects. Furthermore, functional parcellation schemes based on measures of, for example, frequency preference (tonotopy) remain controversial. Here, we propose a 7 Tesla magnetic resonance imaging method that enables the anatomical delineation of auditory cortical areas in vivo and in individual brains, through the high-resolution visualization (0.6 × 0.6 × 0.6 mm(3)) of intracortical anatomical contrast related to myelin. The approach combines the acquisition and analysis of images with multiple MR contrasts (T1, T2*, and proton density). Compared with previous methods, the proposed solution is feasible at high fields and time efficient, which allows collecting myelin-related and functional images within the same measurement session. Our results show that a data-driven analysis of cortical depth-dependent profiles of anatomical contrast allows identifying a most densely myelinated cortical region on the medial Heschl's gyrus. Analyses of functional responses show that this region includes neuronal populations with typical primary functional properties (single tonotopic gradient and narrow frequency tuning), thus indicating that it may correspond to the human homolog of monkey A1.
The human superior temporal plane, the site of the auditory cortex, displays high inter-individual macro-anatomical variation. This questions the validity of curvature-based alignment (CBA) methods ...for in vivo imaging data. Here, we have addressed this issue by developing CBA+, which is a cortical surface registration method that uses prior macro-anatomical knowledge. We validate this method by using cytoarchitectonic areas on 10 individual brains (which we make publicly available). Compared to volumetric and standard surface registration, CBA+ results in a more accurate cytoarchitectonic auditory atlas. The improved correspondence of micro-anatomy following the improved alignment of macro-anatomy validates the superiority of CBA+ compared to CBA. In addition, we use CBA+ to align in vivo and postmortem data. This allows projection of functional and anatomical information collected in vivo onto the cytoarchitectonic areas, which has the potential to contribute to the ongoing debate on the parcellation of the human auditory cortex.
Studying the human subcortical auditory system non-invasively is challenging due to its small, densely packed structures deep within the brain. Additionally, the elaborate three-dimensional (3-D) ...structure of the system can be difficult to understand based on currently available 2-D schematics and animal models. Wfe addressed these issues using a combination of histological data, post mortem magnetic resonance imaging (MRI), and in vivo MRI at 7 Tesla. We created anatomical atlases based on state-of-the-art human histology (BigBrain) and postmortem MRI (50 µm). We measured functional MRI (fMRI) responses to natural sounds and demonstrate that the functional localization of subcortical structures is reliable within individual participants who were scanned in two different experiments. Further, a group functional atlas derived from the functional data locates these structures with a median distance below 2 mm. Using diffusion MRI tractography, we revealed structural connectivity maps of the human subcortical auditory pathway both in vivo (1050 µm isotropic resolution) and post mortem (200 µm isotropic resolution). This work captures current MRI capabilities for investigating the human subcortical auditory system, describes challenges that remain, and contributes novel, openly available data, atlases, and tools for researching the human auditory system.
Recent studies have highlighted the possible contributions of direct connectivity between early sensory cortices to audiovisual integration. Anatomical connections between the early auditory and ...visual cortices are concentrated in visual sites representing the peripheral field of view. Here, we aimed to engage early sensory interactive pathways with simple, far-peripheral audiovisual stimuli (auditory noise and visual gratings). Using a modulation detection task in one modality performed at an 84% correct threshold level, we investigated multisensory interactions by simultaneously presenting weak stimuli from the other modality in which the temporal modulation was barely-detectable (at 55 and 65% correct detection performance). Furthermore, we manipulated the temporal congruence between the cross-sensory streams. We found evidence for an influence of barely-detectable visual stimuli on the response times for auditory stimuli, but not for the reverse effect. These visual-to-auditory influences only occurred for specific phase-differences (at onset) between the modulated audiovisual stimuli. We discuss our findings in the light of a possible role of direct interactions between early visual and auditory areas, along with contributions from the higher-order association cortex. In sum, our results extend the behavioral evidence of audio-visual processing to the far periphery, and suggest - within this specific experimental setting - an asymmetry between the auditory influence on visual processing and the visual influence on auditory processing.
Sensory thalami are central sensory pathway stations for information processing. Their role for human cognition and perception, however, remains unclear. Recent evidence suggests an involvement of ...the sensory thalami in speech recognition. In particular, the auditory thalamus (medial geniculate body, MGB) response is modulated by speech recognition tasks and the amount of this task-dependent modulation is associated with speech recognition abilities. Here, we tested the specific hypothesis that this behaviorally relevant modulation is present in the MGB subsection that corresponds to the primary auditory pathway (i.e., the ventral MGB vMGB). We used ultra-high field 7T fMRI to identify the vMGB, and found a significant positive correlation between the amount of task-dependent modulation and the speech recognition performance across participants within left vMGB, but not within the other MGB subsections. These results imply that modulation of thalamic driving input to the auditory cortex facilitates speech recognition.
Timbre, or sound quality, is a crucial but poorly understood dimension of auditory perception that is important in describing speech, music, and environmental sounds. The present study investigates ...the cortical representation of different timbral dimensions. Encoding models have typically incorporated the physical characteristics of sounds as features when attempting to understand their neural representation with functional MRI. Here we test an encoding model that is based on five subjectively derived dimensions of timbre to predict cortical responses to natural orchestral sounds. Results show that this timbre model can outperform other models based on spectral characteristics, and can perform as well as a complex joint spectrotemporal modulation model. In cortical regions at the medial border of Heschl's gyrus, bilaterally, and regions at its posterior adjacency in the right hemisphere, the timbre model outperforms even the complex joint spectrotemporal modulation model. These findings suggest that the responses of cortical neuronal populations in auditory cortex may reflect the encoding of perceptual timbre dimensions.
•MRI encoding is used to investigate the cortical representation of sound timbre.•We compare a subjective timbre model to spectral/spectrotemporal modulation models.•The timbre model outperforms spectral, but not spectrotemporal modulation models.•The timbre model outperforms all other models in parts of early auditory cortex.•Results support a distributed encoding of timbre dimensions in auditory cortex.
•UHF-fMRI is used to study frequency-specific processing in tinnitus patients.•Control patients are hearing-loss matched to tinnitus patients.•MGB and auditory cortex display reduced frequency ...selectivity with tinnitus.•Thalamocortical and cortico-cortical connectivity is reduced with tinnitus.•UHF-fMRI is relevant for investigating subcortical auditory regions in tinnitus.
Tinnitus is a clinical condition defined by hearing a sound in the absence of an objective source. Early experiments in animal models have suggested that tinnitus stems from an alteration of processing in the auditory system. However, translating these results to humans has proven challenging. One limiting factor has been the insufficient spatial resolution of non-invasive measurement techniques to investigate responses in subcortical auditory nuclei, like the inferior colliculus and the medial geniculate body (MGB). Here we employed ultra-high field functional magnetic resonance imaging (UHF-fMRI) at 7 Tesla to investigate the frequency-specific processing in sub-cortical and cortical regions in a cohort of six tinnitus patients and six hearing loss matched controls. We used task-based fMRI to perform tonotopic mapping and compared the magnitude and tuning of frequency-specific responses between the two groups. Additionally, we used resting-state fMRI to investigate the functional connectivity. Our results indicate frequency-unspecific reductions in the selectivity of frequency tuning that start at the level of the MGB and continue in the auditory cortex, as well as reduced thalamocortical and cortico-cortical connectivity with tinnitus. These findings suggest that tinnitus may be associated with reduced inhibition in the auditory pathway, potentially leading to increased neural noise and reduced functional connectivity. Moreover, these results indicate the relevance of high spatial resolution UHF-fMRI for the investigation of the role of sub-cortical auditory regions in tinnitus.
Auditory cortical processing of complex meaningful sounds entails the transformation of sensory (tonotopic) representations of incoming acoustic waveforms into higher-level sound representations ...(e.g., their category). However, the precise neural mechanisms enabling such transformations remain largely unknown. In the present study, we use functional magnetic resonance imaging (fMRI) and natural sounds stimulation to examine these two levels of sound representation (and their relation) in the human auditory cortex. In a first experiment, we derive cortical maps of frequency preference (tonotopy) and selectivity (tuning width) by mathematical modeling of fMRI responses to natural sounds. The tuning width maps highlight a region of narrow tuning that follows the main axis of Heschl's gyrus and is flanked by regions of broader tuning. The narrowly tuned portion on Heschl's gyrus contains two mirror-symmetric frequency gradients, presumably defining two distinct primary auditory areas. In addition, our analysis indicates that spectral preference and selectivity (and their topographical organization) extend well beyond the primary regions and also cover higher-order and category-selective auditory regions. In particular, regions with preferential responses to human voice and speech occupy the low-frequency portions of the tonotopic map. We confirm this observation in a second experiment, where we find that speech/voice selective regions exhibit a response bias toward the low frequencies characteristic of human voice and speech, even when responding to simple tones. We propose that this frequency bias reflects the selective amplification of relevant and category-characteristic spectral bands, a useful processing step for transforming a sensory (tonotopic) sound image into higher level neural representations.
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