ABSTRACT
Humans and other animals use spatial hearing to rapidly localize events in the environment. However, neural encoding of sound location is a complex process involving the computation and integration of multiple spatial cues that are not represented directly in the sensory organ (the cochlea). Our understanding of these mechanisms has increased enormously in the past few years. Current research is focused on the contribution of animal models for understanding human spatial audition, the effects of behavioural demands on neural sound location encoding, the emergence of a cue-independent location representation in the auditory cortex, and the relationship between single-source and concurrent location encoding in complex auditory scenes. Furthermore, computational modelling seeks to unravel how neural representations of sound source locations are derived from the complex binaural waveforms of real-life sounds. In this article, we review and integrate the latest insights from neurophysiological, neuroimaging and computational modelling studies of mammalian spatial hearing. We propose that the cortical representation of sound location emerges from recurrent processing taking place in a dynamic, adaptive network of early (primary) and higher-order (posterior-dorsal and dorsolateral prefrontal) auditory regions. This cortical network accommodates changing behavioural requirements and is especially relevant for processing the location of real-life, complex sounds and complex auditory scenes.
Subject(s)
Acoustic Stimulation/methods , Auditory Cortex/physiology , Auditory Pathways/physiology , Sound Localization/physiology , Animals , Auditory Cortex/diagnostic imaging , Auditory Pathways/diagnostic imaging , Hearing/physiology , HumansABSTRACT
Across many species, scream calls signal the affective significance of events to other agents. Scream calls were often thought to be of generic alarming and fearful nature, to signal potential threats, with instantaneous, involuntary, and accurate recognition by perceivers. However, scream calls are more diverse in their affective signaling nature than being limited to fearfully alarming a threat, and thus the broader sociobiological relevance of various scream types is unclear. Here we used 4 different psychoacoustic, perceptual decision-making, and neuroimaging experiments in humans to demonstrate the existence of at least 6 psychoacoustically distinctive types of scream calls of both alarming and non-alarming nature, rather than there being only screams caused by fear or aggression. Second, based on perceptual and processing sensitivity measures for decision-making during scream recognition, we found that alarm screams (with some exceptions) were overall discriminated the worst, were responded to the slowest, and were associated with a lower perceptual sensitivity for their recognition compared with non-alarm screams. Third, the neural processing of alarm compared with non-alarm screams during an implicit processing task elicited only minimal neural signal and connectivity in perceivers, contrary to the frequent assumption of a threat processing bias of the primate neural system. These findings show that scream calls are more diverse in their signaling and communicative nature in humans than previously assumed, and, in contrast to a commonly observed threat processing bias in perceptual discriminations and neural processes, we found that especially non-alarm screams, and positive screams in particular, seem to have higher efficiency in speeded discriminations and the implicit neural processing of various scream types in humans.
Subject(s)
Auditory Perception/physiology , Discrimination, Psychological/physiology , Fear/psychology , Voice Recognition/physiology , Adult , Auditory Pathways/diagnostic imaging , Auditory Pathways/physiology , Brain/diagnostic imaging , Female , Humans , Magnetic Resonance Imaging , Male , Pattern Recognition, Physiological/physiology , Recognition, Psychology/physiology , Sex Characteristics , Young AdultABSTRACT
INTRODUCTION: This prospective cohort study aims to investigate the hearing dynamics and the changes in the central auditory pathways in infants with congenital cytomegalovirus (cCMV) infection. MATERIALS AND METHODS: cCMV-infected neonates aged ≤3 weeks old were recruited and underwent clinical and laboratory tests to detect viremia and symptomatic infection, hearing examinations at three and six months of age, and radiological imaging of brain auditory pathways using diffusion tensor imaging. RESULTS: From 26 eligible infants (52 ears), we detected symptomatic infection in nine (34.6%), viremia in 14 (14/25; 56.0%) and sensorineural hearing loss (SNHL) in 14 infants (53.8%). We observed 40 ears (76.9%) with unstable hearing thresholds, 17 (42.5%) of which fluctuated. Hearing fluctuation and progressivity were more common in symptomatic infection (66.7% vs. 14.7%, p<0.001; and 38.9% vs. 2.9%, p=0.002; respectively). A substantial proportion of ears had reduced fractional anisotropy (FA) in the medial geniculate body (59.1%), superior olivary nucleus (45.5%), trapezoid body (40.9%), auditory radiation (36.4%) and inferior colliculus (31.8%). Symptomatic infection was associated with an increased FA in the medial geniculate body (mean difference, MD: 0.12; 95% Confidence Intervals, 95%CI: 0.03, 0.22) and viremia in the inferior colliculus (MD: 0.09; 95%CI: 0.02, 0.16). An FA in the inferior colliculus of ≥0.404 had a sensitivity and specificity of 68.8% and 83.3% in predicting viremia (area under the curve 0.823; 95%CI: 0.633, 1.000, p=0.022). CONCLUSION: SNHL along with its fluctuation and progression are common in cCMV-infected infants. cCMV infection may induce structural changes in the central auditory pathway.
Subject(s)
Auditory Pathways , Cytomegalovirus Infections , Humans , Cytomegalovirus Infections/congenital , Cytomegalovirus Infections/diagnostic imaging , Cytomegalovirus Infections/complications , Cytomegalovirus Infections/physiopathology , Prospective Studies , Female , Male , Infant, Newborn , Auditory Pathways/diagnostic imaging , Auditory Pathways/physiopathology , Hearing Loss, Sensorineural/etiology , Hearing Loss, Sensorineural/virology , Hearing Loss, Sensorineural/physiopathology , Hearing Loss, Sensorineural/diagnostic imaging , Infant , Hearing TestsABSTRACT
Autism spectrum disorder (ASD) is characterised by social communication difficulties. These difficulties have been mainly explained by cognitive, motivational, and emotional alterations in ASD. The communication difficulties could, however, also be associated with altered sensory processing of communication signals. Here, we assessed the functional integrity of auditory sensory pathway nuclei in ASD in three independent functional magnetic resonance imaging experiments. We focused on two aspects of auditory communication that are impaired in ASD: voice identity perception, and recognising speech-in-noise. We found reduced processing in adults with ASD as compared to typically developed control groups (pairwise matched on sex, age, and full-scale IQ) in the central midbrain structure of the auditory pathway (inferior colliculus [IC]). The right IC responded less in the ASD as compared to the control group for voice identity, in contrast to speech recognition. The right IC also responded less in the ASD as compared to the control group when passively listening to vocal in contrast to non-vocal sounds. Within the control group, the left and right IC responded more when recognising speech-in-noise as compared to when recognising speech without additional noise. In the ASD group, this was only the case in the left, but not the right IC. The results show that communication signal processing in ASD is associated with reduced subcortical sensory functioning in the midbrain. The results highlight the importance of considering sensory processing alterations in explaining communication difficulties, which are at the core of ASD.
Subject(s)
Autism Spectrum Disorder , Autistic Disorder , Adult , Auditory Pathways/diagnostic imaging , Autism Spectrum Disorder/diagnostic imaging , Autistic Disorder/complications , Autistic Disorder/diagnostic imaging , Communication , Humans , SpeechABSTRACT
Accumulating evidence shows that auditory cortex (AC) of humans, and other primates, is involved in more complex cognitive processes than feature segregation only, which are shaped by experience-dependent plasticity and thus likely show substantial individual variability. However, thus far, individual variability of ACs has been considered a methodological impediment rather than a phenomenon of theoretical importance. Here, we examined the variability of ACs using intrinsic functional connectivity patterns in humans and macaques. Our results demonstrate that in humans, interindividual variability is greater near the nonprimary than primary ACs, indicating that variability dramatically increases across the processing hierarchy. ACs are also more variable than comparable visual areas and show higher variability in the left than in the right hemisphere, which may be related to the left lateralization of auditory-related functions such as language. Intriguingly, remarkably similar modality differences and lateralization of variability were also observed in macaques. These connectivity-based findings are consistent with a confirmatory task-based functional magnetic resonance imaging analysis. The quantification of variability in auditory function, and the similar findings in both humans and macaques, will have strong implications for understanding the evolution of advanced auditory functions in humans.
Subject(s)
Auditory Cortex/diagnostic imaging , Auditory Pathways/diagnostic imaging , Biological Variation, Individual , Adult , Animals , Auditory Cortex/physiology , Auditory Pathways/physiology , Female , Functional Neuroimaging , Humans , Macaca mulatta , Magnetic Resonance Imaging , Male , Young AdultABSTRACT
The cerebellum, a structure historically associated with motor control, has more recently been implicated in several higher-order auditory-cognitive functions. However, the exact functional pathways that mediate cerebellar influences on auditory cortex (AC) remain unclear. Here, we sought to identify auditory cortico-cerebellar pathways based on intrinsic functional connectivity magnetic resonance imaging. In contrast to previous connectivity studies that principally consider the AC as a single functionally homogenous unit, we mapped the cerebellar connectivity across different parts of the AC. Our results reveal that auditory subareas demonstrating different levels of interindividual functional variability are functionally coupled with distinct cerebellar regions. Moreover, auditory and sensorimotor areas show divergent cortico-cerebellar connectivity patterns, although sensorimotor areas proximal to the AC are often functionally grouped with the AC in previous connectivity-based network analyses. Lastly, we found that the AC can be functionally segmented into highly similar subareas based on either cortico-cerebellar or cortico-cortical functional connectivity, suggesting the existence of multiple parallel auditory cortico-cerebellar circuits that involve different subareas of the AC. Overall, the present study revealed multiple auditory cortico-cerebellar pathways and provided a fine-grained map of AC subareas, indicative of the critical role of the cerebellum in auditory processing and multisensory integration.
Subject(s)
Auditory Cortex/diagnostic imaging , Auditory Pathways/diagnostic imaging , Brain Mapping/methods , Cerebellum/diagnostic imaging , Magnetic Resonance Imaging/methods , Nerve Net/diagnostic imaging , Adult , Auditory Cortex/physiology , Auditory Pathways/physiology , Cerebellum/physiology , Databases, Factual , Female , Humans , Male , Nerve Net/physiology , Young AdultABSTRACT
Congenital blindness has been shown to result in behavioral adaptation and neuronal reorganization, but the underlying neuronal mechanisms are largely unknown. Brain rhythms are characteristic for anatomically defined brain regions and provide a putative mechanistic link to cognitive processes. In a novel approach, using magnetoencephalography resting state data of congenitally blind and sighted humans, deprivation-related changes in spectral profiles were mapped to the cortex using clustering and classification procedures. Altered spectral profiles in visual areas suggest changes in visual alpha-gamma band inhibitory-excitatory circuits. Remarkably, spectral profiles were also altered in auditory and right frontal areas showing increased power in theta-to-beta frequency bands in blind compared with sighted individuals, possibly related to adaptive auditory and higher cognitive processing. Moreover, occipital alpha correlated with microstructural white matter properties extending bilaterally across posterior parts of the brain. We provide evidence that visual deprivation selectively modulates spectral profiles, possibly reflecting structural and functional adaptation.
Subject(s)
Auditory Pathways/physiopathology , Blindness/physiopathology , Frontal Lobe/physiopathology , Visual Pathways/physiopathology , Adult , Auditory Pathways/diagnostic imaging , Auditory Pathways/physiology , Blindness/diagnostic imaging , Diffusion Tensor Imaging , Female , Frontal Lobe/diagnostic imaging , Frontal Lobe/physiology , Humans , Magnetic Resonance Imaging , Magnetoencephalography , Male , Middle Aged , Neuronal Plasticity/physiology , Occipital Lobe/diagnostic imaging , Occipital Lobe/physiology , Occipital Lobe/physiopathology , Visual Pathways/diagnostic imaging , Visual Pathways/physiology , White Matter/diagnostic imaging , White Matter/physiology , White Matter/physiopathology , Young AdultABSTRACT
Despite the multidimensional and temporally fleeting nature of auditory signals we quickly learn to assign novel sounds to behaviorally relevant categories. The neural systems underlying the learning and representation of novel auditory categories are far from understood. Current models argue for a rigid specialization of hierarchically organized core regions that are fine-tuned to extracting and mapping relevant auditory dimensions to meaningful categories. Scaffolded within a dual-learning systems approach, we test a competing hypothesis: the spatial and temporal dynamics of emerging auditory-category representations are not driven by the underlying dimensions but are constrained by category structure and learning strategies. To test these competing models, we used functional Magnetic Resonance Imaging (fMRI) to assess representational dynamics during the feedback-based acquisition of novel non-speech auditory categories with identical dimensions but differing category structures: rule-based (RB) categories, hypothesized to involve an explicit sound-to-rule mapping network, and information integration (II) based categories, involving pre-decisional integration of dimensions via a procedural-based sound-to-reward mapping network. Adults were assigned to either the RB (n = 30, 19 females) or II (n = 30, 22 females) learning tasks. Despite similar behavioral learning accuracies, learning strategies derived from computational modeling and involvements of corticostriatal systems during feedback processing differed across tasks. Spatiotemporal multivariate representational similarity analysis revealed an emerging representation within an auditory sensory-motor pathway exclusively for the II learning task, prominently involving the superior temporal gyrus (STG), inferior frontal gyrus (IFG), and posterior precentral gyrus. In contrast, the RB learning task yielded distributed neural representations within regions involved in cognitive-control and attentional processes that emerged at different time points of learning. Our results unequivocally demonstrate that auditory learners' neural systems are highly flexible and show distinct spatial and temporal patterns that are not dimension-specific but reflect underlying category structures and learning strategies.
Subject(s)
Auditory Cortex/diagnostic imaging , Auditory Perception/physiology , Acoustic Stimulation/methods , Adolescent , Adult , Auditory Pathways/diagnostic imaging , Brain Mapping , Female , Humans , Learning , Magnetic Resonance Imaging , Male , Prefrontal Cortex/diagnostic imaging , Sound , Temporal Lobe/diagnostic imaging , Young AdultABSTRACT
Acoustic trauma damages inner ear neural structures including cochlear hair cells which result in hearing loss and neurotransmitter imbalances within the synapses of the central auditory pathway. Disruption of GABA/glutamate levels underlies, tinnitus, a phantom perception of sound that persists post-exposure to blast noise which may manifest in tandem with acute/chronic loss of hearing. Many putative theories explain tinnitus physiology based on indirect and direct assays in animal models and humans, although there is no comprehensive evidence to explain the phenomenon. Here, GABA/glutamate levels were imaged and quantified in a blast overpressure model of chinchillas using Fourier transform ion cyclotron resonance mass spectrometry imaging. The direct measurement from whole-brain sections identified the relative levels of GABA/glutamate in the central auditory neuraxis centers including the cochlear nucleus, inferior colliculus, and auditory cortex. These preliminary results provide insight on the homeostasis of GABA/glutamate within whole-brain sections of chinchilla for investigation of the pathomechanism of blast-induced tinnitus.
Subject(s)
Auditory Pathways/metabolism , Glutamic Acid/metabolism , Mass Spectrometry , Pressure , gamma-Aminobutyric Acid/metabolism , Animals , Auditory Pathways/diagnostic imaging , Chinchilla , Ions , MaleABSTRACT
Learning complex ordering relationships between sensory events in a sequence is fundamental for animal perception and human communication. While it is known that rhythmic sensory events can entrain brain oscillations at different frequencies, how learning and prior experience with sequencing relationships affect neocortical oscillations and neuronal responses is poorly understood. We used an implicit sequence learning paradigm (an "artificial grammar") in which humans and monkeys were exposed to sequences of nonsense words with regularities in the ordering relationships between the words. We then recorded neural responses directly from the auditory cortex in both species in response to novel legal sequences or ones violating specific ordering relationships. Neural oscillations in both monkeys and humans in response to the nonsense word sequences show strikingly similar hierarchically nested low-frequency phase and high-gamma amplitude coupling, establishing this form of oscillatory coupling-previously associated with speech processing in the human auditory cortex-as an evolutionarily conserved biological process. Moreover, learned ordering relationships modulate the observed form of neural oscillatory coupling in both species, with temporally distinct neural oscillatory effects that appear to coordinate neuronal responses in the monkeys. This study identifies the conserved auditory cortical neural signatures involved in monitoring learned sequencing operations, evident as modulations of transient coupling and neuronal responses to temporally structured sensory input.
Subject(s)
Auditory Cortex/physiology , Auditory Pathways/physiology , Models, Neurological , Neurons/physiology , Neurovascular Coupling , Speech Perception , Verbal Learning , Adult , Animals , Audiometry, Evoked Response , Auditory Cortex/diagnostic imaging , Auditory Pathways/diagnostic imaging , Biological Evolution , Brain Mapping , Female , Functional Neuroimaging , Humans , Macaca mulatta , Magnetic Resonance Imaging , Male , Neural Conduction , Reaction Time , Species Specificity , Task Performance and AnalysisABSTRACT
PURPOSE: It has long been thought that the acoustic radiation (AR) white matter fibre tract from the medial geniculate body of the thalamus to the Heschl's gyrus cannot be reconstructed via single-fibre analysis of clinical diffusion tensor imaging (DTI) scans. A recently developed single-fibre probabilistic method suggests otherwise. The method uses dynamic programming (DP) to compute the most probable paths between two regions of interest. This study aims to observe the ability of single-fibre probabilistic analysis via DP to visualise the AR in clinical DTI scans from legacy pilot cohorts of subjects with normal hearing (NH) and profound hearing loss (HL). METHODS: Single-fibre probabilistic analysis via DP was applied to reconstruct 3D models of the AR in the two cohorts. DTI and T1 data at 1.5 T for subjects with NH (n = 11) and HL (n = 5), as well as 3 T for NH (n = 1) and HL (n = 1), were used. RESULTS: The topographical features of AR previously observed in post-mortem and multi-fibre analyses can be visualised in DTI scans of 16 subjects and 2 atlases with a success rate of 100%. Relative to MNI coordinates, there was no significant difference in the varifold distances between the topography of the tracts in the 1.5 T cohort. CONCLUSION: The AR can be visualised in clinical 1.5 T and 3 T DTI scans using single-fibre probabilistic analysis via DP, hence, the potential for DP to visualise the AR in medical and pre-surgical applications in pathologies such as vestibular schwannoma, multiple sclerosis, thalamic tumours and stroke as well as hearing loss.
Subject(s)
Acoustics , Auditory Pathways/diagnostic imaging , Diffusion Tensor Imaging/methods , Hearing Loss , Thalamus/diagnostic imaging , White Matter , Adult , Female , Humans , Imaging, Three-Dimensional , Male , Middle Aged , Retrospective StudiesABSTRACT
OBJECTIVE: The functional importance of the superior temporal lobe at the level of Heschl's gyrus is well known. However, the organization and function of these cortical areas and the underlying fiber tracts connecting them remain unclear. The goal of this study was to analyze the area formed by the organization of the intersection of Heschl's gyrus-related fiber tracts, which the authors have termed the "Heschl's gyrus fiber intersection area" (HGFIA). METHODS: The subcortical connectivity of Heschl's gyrus tracts was analyzed by white matter fiber dissection and by diffusion tensor imaging tractography. The white matter tracts organized in relation to Heschl's gyrus were isolated in 8 human hemispheres from cadaveric specimens and in 8 MRI studies in 4 healthy volunteers. In addition, these tracts and their functions were described in the surgical cases of left temporal gliomas next to the HGFIA in 6 patients who were awake during surgery and underwent intraoperative electrical stimulation mapping. RESULTS: Five tracts were observed to pass through the HGFIA: the anterior segment of the arcuate fasciculus, the middle longitudinal fasciculus, the acoustic radiation, the inferior fronto-occipital fasciculus, and the optic radiation. In addition, U fibers originating at the level of Heschl's gyrus and heading toward the middle temporal gyrus were identified. CONCLUSIONS: This investigation of the HGFIA, a region where 5 fiber tracts intersect in a relationship with the primary auditory area, provides new insights into the subcortical organization of Wernicke's area. This information is valuable when a temporal surgical approach is planned, in order to assess the surgical risk related to language disturbances.
Subject(s)
Auditory Cortex/diagnostic imaging , Auditory Cortex/physiology , Auditory Pathways/diagnostic imaging , Auditory Pathways/physiology , Auditory Perception/physiology , Language , Adult , Aged , Aged, 80 and over , Auditory Cortex/anatomy & histology , Auditory Pathways/anatomy & histology , Female , Humans , Male , Middle Aged , Nerve Fibers/physiology , Neural Pathways/diagnostic imaging , Neural Pathways/physiologyABSTRACT
Converging evidence from activation, connectivity, and stimulation studies suggests that auditory brain networks are lateralized. Here we show that these findings can be at least partly explained by the asymmetric network embedding of the primary auditory cortices. Using diffusion-weighted imaging in 3 independent datasets, we investigate the propensity for left and right auditory cortex to communicate with other brain areas by quantifying the centrality of the auditory network across a spectrum of communication mechanisms, from shortest path communication to diffusive spreading. Across all datasets, we find that the right auditory cortex is better integrated in the connectome, facilitating more efficient communication with other areas, with much of the asymmetry driven by differences in communication pathways to the opposite hemisphere. Critically, the primacy of the right auditory cortex emerges only when communication is conceptualized as a diffusive process, taking advantage of more than just the topologically shortest paths in the network. Altogether, these results highlight how the network configuration and embedding of a particular region may contribute to its functional lateralization.
Subject(s)
Auditory Cortex/physiology , Auditory Pathways/physiology , Functional Laterality , Acoustic Stimulation , Adult , Aged , Auditory Cortex/diagnostic imaging , Auditory Pathways/diagnostic imaging , Cohort Studies , Communication , Connectome , Diffusion Magnetic Resonance Imaging , Female , Humans , Image Processing, Computer-Assisted , Male , Middle Aged , Young AdultABSTRACT
OBJECTIVES: We report on a patient with sensorineural hearing loss from injury of the auditory radiation following mild TBI, diagnosed by diffusion tensor tractography (DTT). METHOD: A 35-year-old female patient suffered head trauma. While walking in a crosswalk, her left lumbar area was hit by a turning car and she fell to the ground. She was pulled behind the car for several meters while her occipital area repeatedly hit the ground. She complained that she began to feel hearing impairment approximately two weeks after the head trauma, that aggravated over time. Approximately 1.5 years after head trauma, when she visited a university hospital for evaluation of the brain, she complained of severe hearing impairment. To characterize the patient's hearing loss, pure tone audiometry was evaluated in a sound proof room to screen her hearing status for the frequencies 250-8000 Hz. A pure tone threshold in the range of 41-60 dB HL was considered moderate sensorineural hearing loss and 61-80 dB HL severe. However, no abnormality was observed in either ear on physical examination. The patient was diagnosed with bilateral moderate sensorineural hearing loss. RESULTS: On 1.5 year DTT, the auditory radiation was narrowed in both hemispheres. CONCLUSION: Neural injury of the auditory radiation was demonstrated in a patient with sensorineural hearing loss following mild TBI, using DTT.
Subject(s)
Auditory Pathways/diagnostic imaging , Auditory Pathways/injuries , Brain Concussion/complications , Hearing Loss, Sensorineural/etiology , Accidents, Traffic , Adult , Audiometry, Pure-Tone , Auditory Threshold , Brain Concussion/diagnostic imaging , Diffusion Tensor Imaging , Female , Hearing Loss, Sensorineural/diagnostic imaging , Humans , Treatment OutcomeABSTRACT
INTRODUCTION: Tinnitus is the conscious perception of an auditory sensation in the absence of external stimulus. Proposed theories are based on neuroplastic changes that occur due to sensory deprivation. The authors review the relevant literature on functional imaging and neuromodulation of tinnitus and describe potential targets for deep brain stimulation (DBS). MATERIALS AND METHODS: A MEDLINE keyword and Medical Subject Heading term literature search was performed using PubMed for tinnitus, neuromodulation, DBS, transcranial magnetic stimulation, epidural electrode stimulation, intradural electrode stimulation, functional imaging, and connectivity. Data from these reports were extracted and reviewed. RESULTS: Multiple imaging studies are employed to understand the pathophysiology of tinnitus. Abnormal regions and altered connectivity implicated in tinnitus include auditory pathway and limbic structures. Neuromodulation attempts to correct this hyperexcitable state by disrupting these aberrant oscillations and returning activity to baseline. Applied treatment modalities include transcranial magnetic stimulation, epidural/intradural electrode stimulation, and DBS. More recently, modulation of autonomic pathways through vagus nerve stimulation and paired auditory sounds has demonstrated tinnitus improvement via plasticity changes. CONCLUSIONS: DBS shows much promise as a therapeutic option for tinnitus. Stimulation of the auditory pathway, particularly the medial geniculate body, could counteract thalamocortical dysrhythmias and reduce gamma activity implicated in the tinnitus percept. Stimulation of the limbic pathway could decrease attention to and perception of tinnitus. Additional studies, focusing on the involvement of thalamic and limbic structures in the pathophysiology of tinnitus, are needed to support the use of DBS.
Subject(s)
Auditory Pathways/physiopathology , Deep Brain Stimulation/trends , Tinnitus/therapy , Transcranial Magnetic Stimulation/trends , Transcutaneous Electric Nerve Stimulation/trends , Auditory Pathways/diagnostic imaging , Brain/diagnostic imaging , Deep Brain Stimulation/methods , Forecasting , Humans , Magnetic Resonance Imaging/trends , Tinnitus/diagnostic imaging , Tinnitus/physiopathology , Transcranial Magnetic Stimulation/methods , Transcutaneous Electric Nerve Stimulation/methodsABSTRACT
The auditory pathway is widely distributed throughout the brain, and is perhaps one of the most interesting networks in the context of neuroplasticity. Accurate mapping of neural activity in the entire pathway, preferably noninvasively, and with high resolution, could be instrumental for understanding such longitudinal processes. Functional magnetic resonance imaging (fMRI) has clear advantages for such characterizations, as it is noninvasive, provides relatively high spatial resolution and lends itself for repetitive studies, albeit relying on an indirect neurovascular coupling to deliver its information. Indeed, fMRI has been previously used to characterize the auditory pathway in humans and in rats. In the mouse, however, the auditory pathway has insofar only been mapped using manganese-enhanced MRI. Here, we describe a novel setup specifically designed for high-resolution mapping of the mouse auditory pathway using high-field fMRI. Robust and consistent Blood-Oxygenation-Level-Dependent (BOLD) responses were documented along nearly the entire auditory pathway, from the cochlear nucleus (CN), through the superior olivary complex (SOC), nuclei of the lateral lemniscus (LL), inferior colliculus (IC) and the medial geniculate body (MGB). By contrast, clear BOLD responses were not observed in auditory cortex (AC) in this study. Diverse BOLD latencies were mapped ROI- and pixel-wise using coherence analysis, evidencing different averaged BOLD time courses in different auditory centers. Some degree of tonotopy was identified in the IC, SOC, and MGB in the pooled dataset though it could not be assessed per subject due to a lack of statistical power. Given the importance of the mouse model in plasticity studies, animal models, and optogenetics, and fMRI's potential to map dynamic responses to specific cues, this first fMRI study of the mouse auditory pathway paves the way for future longitudinal studies studying brain-wide auditory-related activity in vivo.
Subject(s)
Auditory Cortex/diagnostic imaging , Auditory Pathways/diagnostic imaging , Brain Mapping/methods , Magnetic Resonance Imaging/methods , Acoustic Stimulation , Animals , Female , Male , Mice , Mice, Inbred C57BLABSTRACT
Music learning has received increasing attention in the last decades due to the variety of functions and brain plasticity effects involved during its practice. Most previous reports interpreted the differences between music experts and laymen as the result of training. However, recent investigations suggest that these differences are due to a combination of genetic predispositions with the effect of music training. Here, we tested the relationship of the dorsal auditory-motor pathway with individual behavioural differences in short-term music learning. We gathered structural neuroimaging data from 44 healthy non-musicians (28 females) before they performed a rhythm- and a melody-learning task during a single behavioural session, and manually dissected the arcuate fasciculus (AF) in both hemispheres. The macro- and microstructural organization of the AF (i.e., volume and FA) predicted the learning rate and learning speed in the musical tasks, but only in the right hemisphere. Specifically, the volume of the right anterior segment predicted the synchronization improvement during the rhythm task, the FA in the right long segment was correlated with the learning rate in the melody task, and the volume and FA of the right whole AF predicted the learning speed during the melody task. This is the first study finding a specific relation between different branches within the AF and rhythmic and melodic materials. Our results support the relevant function of the AF as the structural correlate of both auditory-motor transformations and the feedback-feedforward loop, and suggest a crucial involvement of the anterior segment in error-monitoring processes related to auditory-motor learning. These findings have implications for both the neuroscience of music field and second-language learning investigations.
Subject(s)
Auditory Pathways/anatomy & histology , Auditory Perception/physiology , Diffusion Tensor Imaging/methods , Efferent Pathways/anatomy & histology , Learning/physiology , Music , White Matter/anatomy & histology , Adult , Auditory Pathways/diagnostic imaging , Efferent Pathways/diagnostic imaging , Executive Function/physiology , Feedback , Female , Functional Laterality/physiology , Humans , Male , Time Perception/physiology , White Matter/diagnostic imaging , Young AdultABSTRACT
Hypercoupling of activity in speech-perception-specific brain networks has been proposed to play a role in the generation of auditory-verbal hallucinations (AVHs) in schizophrenia; however, it is unclear whether this hypercoupling extends to nonverbal auditory perception. We investigated this by comparing schizophrenia patients with and without AVHs, and healthy controls, on task-based functional magnetic resonance imaging (fMRI) data combining verbal speech perception (SP), inner verbal thought generation (VTG), and nonverbal auditory oddball detection (AO). Data from two previously published fMRI studies were simultaneously analyzed using group constrained principal component analysis for fMRI (group fMRI-CPCA), which allowed for comparison of task-related functional brain networks across groups and tasks while holding the brain networks under study constant, leading to determination of the degree to which networks are common to verbal and nonverbal perception conditions, and which show coordinated hyperactivity in hallucinations. Three functional brain networks emerged: (a) auditory-motor, (b) language processing, and (c) default-mode (DMN) networks. Combining the AO and sentence tasks allowed the auditory-motor and language networks to separately emerge, whereas they were aggregated when individual tasks were analyzed. AVH patients showed greater coordinated activity (deactivity for DMN regions) than non-AVH patients during SP in all networks, but this did not extend to VTG or AO. This suggests that the hypercoupling in AVH patients in speech-perception-related brain networks is specific to perceived speech, and does not extend to perceived nonspeech or inner verbal thought generation.
Subject(s)
Auditory Pathways/physiopathology , Brain/physiopathology , Hallucinations/physiopathology , Magnetic Resonance Imaging , Schizophrenia/physiopathology , Speech Perception/physiology , Adult , Auditory Pathways/diagnostic imaging , Brain/diagnostic imaging , Brain Mapping , Female , Hallucinations/diagnostic imaging , Humans , Language , Male , Neuropsychological Tests , Schizophrenia/diagnostic imagingABSTRACT
Emotion can have diverse effects on behaviour and perception, modulating function in some circumstances, and sometimes having little effect. Recently, it was identified that part of the heterogeneity of emotional effects could be due to a dissociable representation of emotion in dual pathway models of sensory processing. Our previous fMRI experiment using traditional univariate analyses showed that emotion modulated processing in the auditory 'what' but not 'where' processing pathway. The current study aims to further investigate this dissociation using a more recently emerging multi-voxel pattern analysis searchlight approach. While undergoing fMRI, participants localized sounds of varying emotional content. A searchlight multi-voxel pattern analysis was conducted to identify activity patterns predictive of sound location and/or emotion. Relative to the prior univariate analysis, MVPA indicated larger overlapping spatial and emotional representations of sound within early secondary regions associated with auditory localization. However, consistent with the univariate analysis, these two dimensions were increasingly segregated in late secondary and tertiary regions of the auditory processing streams. These results, while complimentary to our original univariate analyses, highlight the utility of multiple analytic approaches for neuroimaging, particularly for neural processes with known representations dependent on population coding.
Subject(s)
Auditory Pathways/physiology , Auditory Perception/physiology , Brain Mapping/methods , Cerebral Cortex/physiology , Emotions/physiology , Space Perception/physiology , Adult , Auditory Pathways/diagnostic imaging , Cerebral Cortex/diagnostic imaging , Female , Humans , Magnetic Resonance Imaging , Male , Sound Localization/physiology , Young AdultABSTRACT
Processing of speech was investigated by using stimuli gradually changing from speech (vowels) to non-speech (spectral rotated vowels). Stimuli were presented in descending levels of vocalization blends, from pure speech to non-speech, through step-wise combinations, resulting in ambiguous versions of the sounds. Participants performed a two-alternative forced choice task: categorization of sounds were made according to whether they contained more speech or non-speech. Performance feedback was presented visually on each trial. Reaction times (RT) after sound presentation, and functional magnetic resonance imaging (fMRI) data during auditory and visual processing, were analyzed. RT data suggested individual differences with a distinct group, good performers, functioning better in distinguishing stimuli with a higher degree of ambiguous blends compared to poor performers, who were not able to distinguish these stimuli correctly. fMRI data confirmed this finding. During auditory stimulation, good performers showed neural activation in the ventral auditory pathway, including the primary auditory cortex and the anterior superior temporal sulcus (responsible for speech processing). Poor performers, in contrast, showed neural activation in the dorsal auditory pathway, including the bilateral superior temporal gyrus. Group differences were also found for visual feedback processing. Differences observed between the groups were interpreted as reflecting different neural processing strategies.