Relationships between human auditory cortical structure and function

The human auditory cortex comprises multiple areas, largely distributed across the supratemporal plane, but the precise number and configuration of auditory areas and their functional significance have not yet been clearly established. In this paper, we discuss recent research concerning architectonic and functional organisation within the human auditory cortex, as well as architectonic and neurophysiological studies in non-human species, which can provide a broad conceptual framework for interpreting functional specialisation in humans. We review the pattern in human auditory cortex of the functional responses to various acoustic cues, such as frequency, pitch, sound level, temporal variation, motion and spatial location, and we discuss their correspondence to what is known about the organisation of the auditory cortex in other primates. There is some neuroimaging evidence of multiple tonotopically organised fields in humans and of functional specialisations of the fields in the processing of different sound features. It is thought that the primary area, on Heschl's gyrus, may have a larger involvement in processing basic sound features, such as frequency and level, and that posterior non-primary areas on the planum temporale may play a larger role in processing more spectrotemporally complex sounds. Ways in which current knowledge of auditory cortical organisation and different data analysis approaches may benefit future functional neuroimaging studies which seek to link auditory cortical structure and function are discussed

Hierarchical Organization in Auditory Cortex of the Cat Using High-Field Functional Magnetic Resonance Imaging

Sensory localization within cortex is a widely accepted and documented principle. Within cortices dedicated to specific sensory information there is further organization. For example, in visual cortices a more detailed functional division and hierarchical organization has been recorded in detail. This organization starts with areas dedicated to analysis of simple visual stimuli. Areas higher in the organization are specialized for processing of progressively more complex stimuli. A similar hierarchical organization has been proposed within auditory cortex and a wealth of evidence supports this hypothesis. In the cat, the initial processing of simple auditory stimuli, such as pure tones, has been well documented in primary auditory cortex (A1) which is also the recipient of the largest projection from the thalamus. This indicates that at least the initial stages of a hierarchy exist within auditory cortex. Until now it has been difficult to investigate the remaining hierarchy in its entirety because of methodological limitations. In the present set of investigations the use of functional magnetic resonance imaging (fMRI) facilitated the investigation of auditory cortex of the cat in its entirety. Results from these investigations support the proposed hierarchy in auditory cortex in the cat with lower cortical areas selectively responding to more simple stimuli while higher areas are progressively more responsive to complex stimuli

Representation of Sound Objects within Early-Stage Auditory Areas: A Repetition Effect Study Using 7T fMRI.

Environmental sounds are highly complex stimuli whose recognition depends on the interaction of top-down and bottom-up processes in the brain. Their semantic representations were shown to yield repetition suppression effects, i. e. a decrease in activity during exposure to a sound that is perceived as belonging to the same source as a preceding sound. Making use of the high spatial resolution of 7T fMRI we have investigated the representations of sound objects within early-stage auditory areas on the supratemporal plane. The primary auditory cortex was identified by means of tonotopic mapping and the non-primary areas by comparison with previous histological studies. Repeated presentations of different exemplars of the same sound source, as compared to the presentation of different sound sources, yielded significant repetition suppression effects within a subset of early-stage areas. This effect was found within the right hemisphere in primary areas A1 and R as well as two non-primary areas on the antero-medial part of the planum temporale, and within the left hemisphere in A1 and a non-primary area on the medial part of Heschl's gyrus. Thus, several, but not all early-stage auditory areas encode the meaning of environmental sounds

Representation of statistical sound properties in human auditory cortex

The work carried out in this doctoral thesis investigated the representation of statistical sound properties in human auditory cortex. It addressed four key aspects in auditory neuroscience: the representation of different analysis time windows in auditory cortex; mechanisms for the analysis and segregation of auditory objects; information-theoretic constraints on pitch sequence processing; and the analysis of local and global pitch patterns. The majority of the studies employed a parametric design in which the statistical properties of a single acoustic parameter were altered along a continuum, while keeping other sound properties fixed. The thesis is divided into four parts. Part I (Chapter 1) examines principles of anatomical and functional organisation that constrain the problems addressed. Part II (Chapter 2) introduces approaches to digital stimulus design, principles of functional magnetic resonance imaging (fMRI), and the analysis of fMRI data. Part III (Chapters 3-6) reports five experimental studies. Study 1 controlled the spectrotemporal correlation in complex acoustic spectra and showed that activity in auditory association cortex increases as a function of spectrotemporal correlation. Study 2 demonstrated a functional hierarchy of the representation of auditory object boundaries and object salience. Studies 3 and 4 investigated cortical mechanisms for encoding entropy in pitch sequences and showed that the planum temporale acts as a computational hub, requiring more computational resources for sequences with high entropy than for those with high redundancy. Study 5 provided evidence for a hierarchical organisation of local and global pitch pattern processing in neurologically normal participants. Finally, Part IV (Chapter 7) concludes with a general discussion of the results and future perspectives

The mechanisms of tinnitus: perspectives from human functional neuroimaging

In this review, we highlight the contribution of advances in human neuroimaging to the current understanding of central mechanisms underpinning tinnitus and explain how interpretations of neuroimaging data have been guided by animal models. The primary motivation for studying the neural substrates of tinnitus in humans has been to demonstrate objectively its representation in the central auditory system and to develop a better understanding of its diverse pathophysiology and of the functional interplay between sensory, cognitive and affective systems. The ultimate goal of neuroimaging is to identify subtypes of tinnitus in order to better inform treatment strategies. The three neural mechanisms considered in this review may provide a basis for TI classification. While human neuroimaging evidence strongly implicates the central auditory system and emotional centres in TI, evidence for the precise contribution from the three mechanisms is unclear because the data are somewhat inconsistent. We consider a number of methodological issues limiting the field of human neuroimaging and recommend approaches to overcome potential inconsistency in results arising from poorly matched participants, lack of appropriate controls and low statistical power

A primate model of human cortical analysis of auditory objects

PhD ThesisThe anatomical organization of the auditory cortex in old world monkeys is similar to that in humans. But how good are monkeys as a model of human cortical analysis of auditory objects? To address this question I explore two aspects of auditory objectprocessing: segregation and timbre. Auditory segregation concerns the ability of animals to extract an auditory object of relevance from a background of competing sounds. Timbre is an aspect of object identity distinct from pitch. In this work, I study these phenomena in rhesus macaques using behaviour and functional magnetic resonance imaging (fMRI). I specifically manipulate one dimension of timbre, spectral flux: the rate of change of spectral energy.I present this thesis in five chapters. Chapter 1 presents background on auditory processing, macaque auditory cortex, models of auditory segregation, and dimensions of timbre. Chapter 2 presents an introduction to fMRI, the design of the fMRI experiments and analysis of fMRI data, and macaque behavioural training techniques employed. Chapter 3 presents results from the fMRI and behavioural experiments on macaques using a stochastic figure-ground stimulus. Chapter 4 presents the results from the fMRI experiment in macaques using spectral flux stimulus. Chapter 5 concludes with a general discussion of the results from both the studies and some future directions for research.In summary, I show that there is a functional homology between macaques and humans in the cortical processing of auditory figure-ground segregation. However, there is no clear functional homology in the processing of spectral flux between these species. So I conclude that, despite clear similarities in the organization of the auditory cortex and processing of auditory object segregation, there are important differences in how complex cues associated with auditory object identity are processed in the macaque and human auditory brains.Wellcome Trust U

Common Fronto-temporal Effective Connectivity in Humans and Monkeys

Cognitive pathways supporting human language and declarative memory are thought to have uniquely evolutionarily differentiated in our species. However, cross-species comparisons are missing on site-specific effective connectivity between regions important for cognition. We harnessed a new approach using functional imaging to visualize the impact of direct electrical brain stimulation in human neurosurgery patients. Applying the same approach with macaque monkeys, we found remarkably comparable patterns of effective connectivity between auditory cortex and ventro-lateral prefrontal cortex (vlPFC) and parahippocampal cortex in both species. Moreover, in humans electrical tractography revealed rapid evoked potentials in vlPFC from stimulating auditory cortex and speech sounds drove vlPFC, consistent with prior evidence in monkeys of direct projections from auditory cortex to vocalization responsive regions in vlPFC. The results identify a common effective connectivity signature that from auditory cortex is equally direct to vlPFC and indirect to the hippocampus (via parahippocampal cortex) in human and nonhuman primates

Mapping tonotopic organization in human temporal cortex: representational similarity analysis in EMEG source space.

A wide variety of evidence, from neurophysiology, neuroanatomy, and imaging studies in humans and animals, suggests that human auditory cortex is in part tonotopically organized. Here we present a new means of resolving this spatial organization using a combination of non-invasive observables (EEG, MEG, and MRI), model-based estimates of spectrotemporal patterns of neural activation, and multivariate pattern analysis. The method exploits both the fine-grained temporal patterning of auditory cortical responses and the millisecond scale temporal resolution of EEG and MEG. Participants listened to 400 English words while MEG and scalp EEG were measured simultaneously. We estimated the location of cortical sources using the MRI anatomically constrained minimum norm estimate (MNE) procedure. We then combined a form of multivariate pattern analysis (representational similarity analysis) with a spatiotemporal searchlight approach to successfully decode information about patterns of neuronal frequency preference and selectivity in bilateral superior temporal cortex. Observed frequency preferences in and around Heschl's gyrus matched current proposals for the organization of tonotopic gradients in primary acoustic cortex, while the distribution of narrow frequency selectivity similarly matched results from the fMRI literature. The spatial maps generated by this novel combination of techniques seem comparable to those that have emerged from fMRI or ECOG studies, and a considerable advance over earlier MEG results.This work was supported by a European Research Council Advanced Grant (230570 Neurolex) and Medical Research Council Cognition and Brain Sciences Unit funding to William Marslen-Wilson (U.1055.04.002.00001.01). The involvement of Li Su was also partly supported by the NIHR Biomedical Research Centre and Biomedical Research Unit in Dementia based at Cambridge University Hospitals NHS Foundation Trust.This is the final published article. It originally appeared at http://journal.frontiersin.org/Journal/10.3389/fnins.2014.00368/full

Auditory sequence processing reveals evolutionarily conserved regions of frontal cortex in macaques and humans.

An evolutionary account of human language as a neurobiological system must distinguish between human-unique neurocognitive processes supporting language and evolutionarily conserved, domain-general processes that can be traced back to our primate ancestors. Neuroimaging studies across species may determine whether candidate neural processes are supported by homologous, functionally conserved brain areas or by different neurobiological substrates. Here we use functional magnetic resonance imaging in Rhesus macaques and humans to examine the brain regions involved in processing the ordering relationships between auditory nonsense words in rule-based sequences. We find that key regions in the human ventral frontal and opercular cortex have functional counterparts in the monkey brain. These regions are also known to be associated with initial stages of human syntactic processing. This study raises the possibility that certain ventral frontal neural systems, which play a significant role in language function in modern humans, originally evolved to support domain-general abilities involved in sequence processing

The effect of listening tasks and motor responding on activation in The auditory cortex

Previous human functional magnetic resonance imaging (fMRI) research has shown that activation in the auditory cortex (AC) is strongly modulated by motor influences. Other fMRI studies have indicated that the AC is also modulated by attention-engaging listening tasks. How these motor- and task-related activation modulations relate to each other has, however, not been previously studied. The current understanding of the functional organization of the human AC is strongly based on primate models. However, some authors have recently questioned the correspondence between the monkey and human cognitive systems, and whether the monkey AC can be used as a model for the human AC. Further, it is unknown whether active listening modulates activations similarly in the human and nonhuman primate AC. Thus, non-human primate fMRI studies are important. Yet, such fMRI studies have been previously impeded by the difficulty in teaching tasks to non-human primates. The present thesis consists of three studies in which fMRI was used both to investigate the relationship between the effects related to active listening and motor responding in the human AC and to investigate task-related activation modulations in the monkey AC. Study I investigated the effect of manual responding on activation in the human AC during auditory and visual tasks, whereas Study II focused on the question whether auditory-motor effects interact with those related to active listening tasks in the AC and adjacent regions. In Study III, a novel paradigm was developed and used during fMRI to investigate auditory task-dependent modulations in the monkey AC. The results of Study I showed that activation in the AC in humans is strongly suppressed when subjects respond to targets using precision or power grips during both visual and auditory tasks. AC activation was also modulated by grip type during the auditory task but not during the visual task (with identical stimuli and motor responses). These manual-motor effects were distinct from general attention-related modulations revealed by comparing activation during auditory and visual tasks. Study II showed that activation in widespread regions in the AC and inferior parietal lobule (IPL) depends on whether subjects respond to target vowel pairs using vocal or manual responses. Furthermore, activation in the posterior AC and the IPL depends on whether subjects respond by overtly repeating the last vowel of a target pair or by producing a given response vowel. Discrimination tasks activated superior temporal gyrus (STG) regions more strongly than 2-back tasks, while the IPL was activated more strongly by 2-back tasks. These task-related (discrimination vs. 2-back) modulations were distinct from the response type effects in the AC. However, task and motor-response-type effects interacted in the IPL. Together the results of Studies I and II support the view that operations in the AC are shaped by its connections with motor cortical regions and that regions in the posterior AC are important in auditory-motor integration. Furthermore, these studies also suggest that the task, motor-response-type and vocal-response-type effects are caused by independent mechanisms in the AC. In Study III, a novel reward-cue paradigm was developed to teach macaque monkeys to perform an auditory task. Using this paradigm monkeys learned to perform an auditory task in a few weeks, whereas in previous studies auditory task training has required months or years of training. This new paradigm was then used during fMRI to measure activation in the monkey AC during active auditory task performance. The results showed that activation in the monkey AC is modulated during this task in a similar way as previously seen in human auditory attention studies. The findings of Study III provide an important step in bridging the gap between human and animal studies of the AC.Tidigare forskning med funktionell magnetresonanstomografi (fMRI) har visat att aktiveringen i hörselhjärnbarken hos människor är starkt påverkad av motoriken. Andra fMRI-studier visar att aktiveringen i hörselhjärnbarken också påverkas av uppgifter som kräver aktivt lyssnande. Man vet ändå inte hur dessa motoriska och uppgiftsrelaterade effekter hänger ihop. Den nuvarande uppfattningen om hörselhjärnbarkens funktionella struktur hos människan är starkt påverkad av primatmodeller. Däremot har en del forskare nyligen ifrågasatt om apors kognitiva system motsvarar människans, och specifikt huruvida apans hörselhjärnbark kan användas som modell för människans. Dessutom vet man inte om aktivt lyssnande påverkar aktivering i hörselhjärnbarken hos apor på samma sätt som hos människor. Därför är fMRI-studier på apor viktiga. Sådana fMRI-studier har emellertid tidigare hindrats av svårigheten att lära apor att göra uppgifter. Denna doktorsavhandling utgörs av tre studier där man använde fMRI för att undersöka hur effekter som är relaterade till aktivt lyssnande och motorik förhåller sig till varandra i hörselhjärnbarken hos människan och hur aktiva uppgifter påverkar aktiveringar i hörselhjärnbarken hos apor. I Studie I undersöktes hur aktiveringen i hörselhjärnbarken hos människan påverkades medan försökspersonerna utförde auditiva och visuella uppgifter och gav sina svar manuellt. Studie II fokuserade på huruvida audiomotoriska effekter och effekter relaterade till aktiva hörseluppgifter samspelade i hörselhjärnbarken och dess omnejd. I Studie III utvecklades ett nytt försöksparadigm som sedermera användes för att undersöka auditiva uppgiftsrelaterade aktiveringar i hörselhjärnbarken hos apor. Resultaten av Studie I visade att aktiveringen i hörselhjärnbarken dämpas starkt när försökspersonerna reagerar på målstimulus med precisions- och styrkegrepp både vid auditiva och visuella uppgifter. Aktivering i hörselhjärnbarken påverkas också av typen av grepp då försökspersonerna utför auditiva uppgifter men inte då de utför visuella uppgifter (med identiska stimuli och motoriska reaktioner). Dessa manuellt-motoriska effekter kunde särskiljas från allmänna uppmärksamhetsrelaterade effekter, vilka kom fram då man jämförde aktiveringen under auditiva och visuella uppgifter. Typen av motoriska reaktioner, dvs. hur försökspersonerna reagerade på målstimuli (genom att reagera med händerna eller att uttala ljud) påverkade aktiveringen i stora områden i hörselhjärnbarken och lobulus parietale inferior (IPL) i Studie II. Aktiveringen i den bakre delen av hörselhjärnbarken och IPL påverkades också av om försökspersonen upprepade målstimulusens sista vokal eller svarade genom att uttala en given responsvokal. Diskriminationsuppgifter aktiverade gyrus temporale superior mera än 2-back (minnes) -uppgifter, medan IPL aktiverades mera av 2-back -uppgifterna. Dessa uppgiftsrelaterade (diskrimination vs. 2-back) påverkningar var oberoende av effekter som hade att göra med reaktionstypen i hörselhjärnbarken. Däremot fanns det ett samspel mellan uppgift och motoriska effekter i IPL. Tillsammans stärker resultaten från Studie I och II uppfattningen att funktioner inom hörselhjärnbarken är starkt beroende av dess sammankoppling med den motoriska hjärnbarken, och att bakre delarna av hörselhjärnbarken är viktiga för audiomotorisk integration. Dessa studier visar därtill att uppgiftsrelaterade, motoriska och uttalsrelaterade effekter produceras av oberoende mekanismer i hörselhjärnbarken. I Studie III utvecklades ett nytt försöksparadigm som var baserat på belöningssignaler. Med detta försöksparadigm lärdes makakapor att utföra en auditiv uppgift. I Studie III lärde sig makakaporna uppgiften inom ett par veckor, medan inlärningen av auditiva uppgifter i tidigare studier har tagit upp till flera år. Detta paradigm användes sedan med hjälp av fMRI för att mäta aktivering inom hörselhjärnbarken hos apor, medan aporna utförde aktiva auditiva uppgifter. Resultaten visar att aktiveringen i hörselhjärnbarken hos apor påverkas av uppgifter på liknande sätt som man tidigare har visat i människoforskning. Fynden i Studie II är ett viktigt framsteg för att kunna överbygga gapet mellan människostudier och djurstudier gällande hörselhjärnbarken