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

Interaction of the effects associated with auditory-motor integration and attention-engaging listening tasks

A number of previous studies have implicated regions in posterior auditory cortex (AC) in auditory-motor integration during speech production. Other studies, in turn, have shown that activation in AC and adjacent regions in the inferior parietal lobule (IPL) is strongly modulated during active listening and depends on task requirements. The present fMRI study investigated whether auditory-motor effects interact with those related to active listening tasks in AC and IPL. In separate task blocks, our subjects performed either auditory discrimination or 2-back memory tasks on phonemic or nonphonemic vowels. They responded to targets by either overtly repeating the last vowel of a target pair, overtly producing a given response vowel, or by pressing a response button. We hypothesized that the requirements for auditory-motor integration, and the associated activation, would be stronger during repetition than production responses and during repetition of nonphonemic than phonemic vowels. We also hypothesized that if auditory-motor effects are independent of task-dependent modulations, then the auditory-motor effects should not differ during discrimination and 2-back tasks. We found that activation in AC and IPL was significantly modulated by task (discrimination vs. 2-back), vocal-response type (repetition vs. production), and motor-response type (vocal vs. button). Motor-response and task effects interacted in IPL but not in AC. Overall, the results support the view that regions in posterior AC are important in auditory-motor integration. However, the present study shows that activation in wide AC and IPL regions is modulated by the motor requirements of active listening tasks in a more general manner. Further, the results suggest that activation modulations in AC associated with attention-engaging listening tasks and those associated with auditory-motor performance are mediated by independent mechanisms.Peer reviewe

Reward cues readily direct monkeys’ auditory performance resulting in broad auditory cortex modulation and interaction with sites along cholinergic and dopaminergic pathways

In natural settings, the prospect of reward often influences the focus of our attention, but how cognitive and motivational systems influence sensory cortex is not well understood. Also, challenges in training nonhuman animals on cognitive tasks complicate cross-species comparisons and interpreting results on the neurobiological bases of cognition. Incentivized attention tasks could expedite training and evaluate the impact of attention on sensory cortex. Here we develop an Incentivized Attention Paradigm (IAP) and use it to show that macaque monkeys readily learn to use auditory or visual reward cues, drastically influencing their performance within a simple auditory task. Next, this paradigm was used with functional neuroimaging to measure activation modulation in the monkey auditory cortex. The results show modulation of extensive auditory cortical regions throughout primary and non-primary regions, which although a hallmark of attentional modulation in human auditory cortex, has not been studied or observed as broadly in prior data from nonhuman animals. Psycho-physiological interactions were identified between the observed auditory cortex effects and regions including basal forebrain sites along acetylcholinergic and dopaminergic pathways. The findings reveal the impact and regional interactions in the primate brain during an incentivized attention engaging auditory task.Peer reviewe

Brain activity during shadowing of audiovisual cocktail party speech, contributions of auditory-motor integration and selective attention

Selective listening to cocktail-party speech involves a network of auditory and inferior frontal cortical regions. However, cognitive and motor cortical regions are differentially activated depending on whether the task emphasizes semantic or phonological aspects of speech. Here we tested whether processing of cocktail-party speech differs when participants perform a shadowing (immediate speech repetition) task compared to an attentive listening task in the presence of irrelevant speech. Participants viewed audiovisual dialogues with concurrent distracting speech during functional imaging. Participants either attentively listened to the dialogue, overtly repeated (i.e., shadowed) attended speech, or performed visual or speech motor control tasks where they did not attend to speech and responses were not related to the speech input. Dialogues were presented with good or poor auditory and visual quality. As a novel result, we show that attentive processing of speech activated the same network of sensory and frontal regions during listening and shadowing. However, in the superior temporal gyrus (STG), peak activations during shadowing were posterior to those during listening, suggesting that an anterior-posterior distinction is present for motor vs. perceptual processing of speech already at the level of the auditory cortex. We also found that activations along the dorsal auditory processing stream were specifically associated with the shadowing task. These activations are likely to be due to complex interactions between perceptual, attention dependent speech processing and motor speech generation that matches the heard speech. Our results suggest that interactions between perceptual and motor processing of speech relies on a distributed network of temporal and motor regions rather than any specific anatomical landmark as suggested by some previous studies.Peer reviewe

Interaction of the effects associated with auditory-motor integration and attention-engaging listening tasks

A number of previous studies have implicated regions in posterior auditory cortex (AC) in auditory-motor integration during speech production. Other studies, in turn, have shown that activation in AC and adjacent regions in the inferior parietal lobule (IPL) is strongly modulated during active listening and depends on task requirements. The present fMRI study investigated whether auditory-motor effects interact with those related to active listening tasks in AC and IPL. In separate task blocks, our subjects performed either auditory discrimination or 2-back memory tasks on phonemic or nonphonemic vowels. They responded to targets by either overtly repeating the last vowel of a target pair, overtly producing a given response vowel, or by pressing a response button. We hypothesized that the requirements for auditory-motor integration, and the associated activation, would be stronger during repetition than production responses and during repetition of nonphonemic than phonemic vowels. We also hypothesized that if auditory-motor effects are independent of task-dependent modulations, then the auditory-motor effects should not differ during discrimination and 2-back tasks. We found that activation in AC and IPL was significantly modulated by task (discrimination vs. 2-back), vocal-response type (repetition vs. production), and motor-response type (vocal vs. button). Motor-response and task effects interacted in IPL but not in AC. Overall, the results support the view that regions in posterior AC are important in auditory-motor integration. However, the present study shows that activation in wide AC and IPL regions is modulated by the motor requirements of active listening tasks in a more general manner. Further, the results suggest that activation modulations in AC associated with attention-engaging listening tasks and those associated with auditory-motor performance are mediated by independent mechanisms.</p

Modulation of brain activity by selective attention to audiovisual dialogues

In real-life noisy situations, we can selectively attend to conversations in the presence of irrelevant voices, but neurocognitive mechanisms in such natural listening situations remain largely unexplored. Previous research has shown distributed activity in the mid superior temporal gyrus (STG) and sulcus (STS) while listening to speech and human voices, in the posterior STS and fusiform gyrus when combining auditory, visual and linguistic information, as well as in left-hemisphere temporal and frontal cortical areas during comprehension. In the present functional magnetic resonance imaging (fMRI) study, we investigated how selective attention modulates neural responses to naturalistic audiovisual dialogues. Our healthy adult participants (N = 15) selectively attended to video-taped dialogues between a man and woman in the presence of irrelevant continuous speech in the background. We modulated the auditory quality of dialogues with noise vocoding and their visual quality by masking speech-related facial movements. Both increased auditory quality and increased visual quality were associated with bilateral activity enhancements in the STG/STS. In addition, decreased audiovisual stimulus quality elicited enhanced fronto-parietal activity, presumably reflecting increased attentional demands. Finally, attention to the dialogues, in relation to a control task where a fixation cross was attended and the dialogue ignored, yielded enhanced activity in the left planum polare, angular gyrus, the right temporal pole, as well as in the orbitofrontal/ventromedial prefrontal cortex and posterior cingulate gyrus. Our findings suggest that naturalistic conversations effectively engage participants and reveal brain networks related to social perception in addition to speech and semantic processing networks.Peer reviewe

Reward cues readily direct monkeys' auditory performance resulting in broad auditory cortex modulation and interaction with sites along cholinergic and dopaminergic pathways

In natural settings, the prospect of reward often influences the focus of our attention, but how cognitive and motivational systems influence sensory cortex is not well understood. Also, challenges in training nonhuman animals on cognitive tasks complicate cross-species comparisons and interpreting results on the neurobiological bases of cognition. Incentivized attention tasks could expedite training and evaluate the impact of attention on sensory cortex. Here we develop an Incentivized Attention Paradigm (IAP) and use it to show that macaque monkeys readily learn to use auditory or visual reward cues, drastically influencing their performance within a simple auditory task. Next, this paradigm was used with functional neuroimaging to measure activation modulation in the monkey auditory cortex. The results show modulation of extensive auditory cortical regions throughout primary and non-primary regions, which although a hallmark of attentional modulation in human auditory cortex, has not been studied or observed as broadly in prior data from nonhuman animals. Psycho-physiological interactions were identified between the observed auditory cortex effects and regions including basal forebrain sites along acetylcholinergic and dopaminergic pathways. The findings reveal the impact and regional interactions in the primate brain during an incentivized attention engaging auditory task

The effect of precision and power grips on activations in human auditory cortex

The neuroanatomical pathways interconnecting auditory and motor cortices play a key role in current models of human auditory cortex (AC). Evidently, auditory-motor interaction is important in speech and music production, but the significance of these cortical pathways in other auditory processing is not well known. We investigated the general effects of motor responding on AC activations to sounds during auditory and visual tasks (motor regions were not imaged). During all task blocks, subjects detected targets in the designated modality, reported the relative number of targets at the end of the block, and ignored the stimuli presented in the opposite modality. In each block, they were also instructed to respond to targets either using a precision grip, power grip, or to give no overt target responses. We found that motor responding strongly modulated AC activations. First, during both visual and auditory tasks, activations in widespread regions of AC decreased when subjects made precision and power grip responses to targets. Second, activations in AC were modulated by grip type during the auditory but not during the visual task. Further, the motor effects were distinct from the present strong attention-related modulations in AC. These results are consistent with the idea that operations in AC are shaped by its connections with motor cortical regions.Peer reviewe

Brain Responses to Peer Feedback in Social Media Are Modulated by Valence in Late Adolescence

Previous studies have examined the neural correlates of receiving negative feedback from peers during virtual social interaction in young people. However, there is a lack of studies applying platforms adolescents use in daily life. In the present study, 92 late-adolescent participants performed a task that involved receiving positive and negative feedback to their opinions from peers in a Facebook-like platform, while brain activity was measured using functional magnetic resonance imaging (fMRI). Peer feedback was shown to activate clusters in the ventrolateral prefrontal cortex (VLPFC), medial prefrontal cortex (MPFC), superior temporal gyrus and sulcus (STG/STS), and occipital cortex (OC). Negative feedback was related to greater activity in the VLPFC, MPFC, and anterior insula than positive feedback, replicating previous findings on peer feedback and social rejection. Real-life habits of social media use did not correlate with brain responses to negative feedback.Peer reviewe

Early life stress is associated with the default mode and fronto-limbic network connectivity among young adults

Exposure to early life stress (ELS) is associated with a variety of detrimental psychological and neurodevelopmental effects. Importantly, ELS has been associated with regional alterations and aberrant connectivity in the structure and functioning of brain regions involved in emotion processing and self-regulation, creating vulnerability to mental health problems. However, longitudinal research regarding the impact of ELS on functional connectivity between brain regions in the default mode network (DMN) and fronto-limbic network (FLN), both implicated in emotion-related processes, is relatively scarce. Neuroimaging research on ELS has mostly focused on single nodes or bi-nodal connectivity instead of functional networks. We examined how ELS is associated with connectivity patterns within the DMN and FLN during rest in early adulthood. The participants (n = 86; 47 females) in the current functional magnetic resonance imaging (fMRI) study were young adults (18-21 years old) whose families had participated in a longitudinal study since pregnancy. ELS was assessed both prospectively (parental reports of family relationship problems and mental health problems during pregnancy and infancy) and retrospectively (self-reported adverse childhood experiences). Inter-subject representational similarity analysis (IS-RSA) and multivariate distance matrix regression (MDMR) were used to analyze the association between ELS and the chosen networks. The IS-RSA results suggested that prospective ELS was associated with complex alterations within the DMN, and that retrospective ELS was associated with alterations in the FLN. MDMR results, in turn, suggested that that retrospective ELS was associated with DMN connectivity. Mean connectivity of the DMN was also associated with retrospective ELS. Analyses further showed that ELS-related alterations in the FLN were associated with increased connectivity between the prefrontal and limbic regions, and between different prefrontal regions. These results suggest that exposure to ELS in infancy might have long-lasting influences on functional brain connectivity that persist until early adulthood. Our results also speak for the importance of differentiating prospective and retrospective assessment methods to understand the specific neurodevelopmental effects of ELS.Peer reviewe