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Auditory dorsal pathway

From EverybodyWiki Bios & Wiki

Dual stream connectivity between the auditory cortex and frontal lobe of monkeys and humans. Top: The auditory cortex of the monkey (left) and human (right) is schematically depicted on the supratemporal plane and observed from above (with the parieto- frontal operculi removed). Bottom: The brain of the monkey (left) and human (right) is schematically depicted and displayed from the side. Orange frames mark the region of the auditory cortex, which is displayed in the top sub-figures. Top and Bottom: Blue colors mark regions affiliated with the ADS, and red colors mark regions affiliated with the AVS (dark red and blue regions mark the primary auditory fields). Abbreviations: AMYG-amygdala, HG-Heschl's gyrus, FEF-frontal eye field, IFG-inferior frontal gyrus, INS-insula, IPS-intra parietal sulcus, MTG-middle temporal gyrus, PC-pitch center, PMd-dorsal premotor cortex, PP-planum polare, PT-planum temporale, TP-temporal pole, Spt-sylvian parietal-temporal, pSTG/mSTG/aSTG-posterior/middle/anterior superior temporal gyrus, CL/ ML/AL/RTL-caudo-/middle-/antero-/rostrotemporal-lateral belt area, CPB/RPB-caudal/rostral parabelt fields. Used with permission from Poliva O. From where to what: a neuroanatomically based evolutionary model of the emergence of speech in humans.

The auditory dorsal stream (ADS) is a neuroanatomical pathway in the primate's brain that connects the primary auditory cortex with the parietal lobe and the frontal lobe. In monkeys, the primary region associated with this pathway is the intraparietal sulcus, and the primary region in the frontal lobe is the dorsolateral prefrontal cortex and the dorsal premotor region. The primary function of this pathway is non-human primates is sound localization. A common moniker for this neuroanatomical pathway is the auditory 'where' pathway. In humans, the primary parietal region is the inferior parietal lobule and temporo-parietal region, and the primary frontal lobe region is the inferior frontal gyrus. In humans, this pathway was ascribed with many functions (in addition to sound localization), such as: integration of speech with lip-movements, speech production, speech mimicry, phonological working memory and phnological long-term memory. Damage to the parietal lobe is associated with the disorder conduction aphasia, a disorder characterized with impaired ability to repeat sentences and nonsense words. Damage to the inferior frontal gyrus is associated with Broca's aphasia.

Auditory dorsal stream[edit]

Sound localization[edit]

The most established role of the ADS is with audiospatial processing. This is evidenced via studies that recorded neural activity from the auditory cortex of monkeys, and correlated the strongest selectivity to changes in sound location with the posterior auditory fields (areas CM-CL), intermediate selectivity with primary area A1, and very weak selectivity with the anterior auditory fields.[1][2][3][4][5] In humans, behavioral studies of brain damaged patients[6][7] and EEG recordings from healthy participants[8] demonstrated that sound localization is processed independently of sound recognition, and thus is likely independent of processing in the AVS. Consistently, a working memory study[9] reported two independent working memory storage spaces, one for acoustic properties and one for locations. Functional imaging studies that contrasted sound discrimination and sound[10][11][12][13][14][15] localization reported a correlation between sound discrimination and activation in the mSTG-aSTG, and correlation between sound localization and activation in the pSTG and PT, with some studies further reporting of activation in the Spt-IPL region and frontal lobe.[16][17][18] Some fMRI studies also reported that the activation in the pSTG and Spt-IPL regions increased when individuals perceived sounds in motion.[19][20][21] EEG studies using source-localization also identified the pSTG-Spt region of the ADS as the sound localization processing center[22][23] A combined fMRI and MEG study corroborated the role of the ADS with audiospatial processing by demonstrating that changes in sound location resulted in activation spreading from Heschl's gyrus posteriorly along the pSTG and terminating in the IPL.[24] In another MEG study, the IPL and frontal lobe were shown active during maintenance of sound locations in working memory.[25]

Guidance of eye movements[edit]

In addition to localizing sounds, the ADS appears also to encode the sound location in memory, and to use this information for guiding eye movements. Evidence for the role of the ADS in encoding sounds into working memory is provided via studies that trained monkeys in a delayed matching to sample task, and reported of activation in areas CM-CL[26] and IPS[27][28] during the delay phase. Influence of this spatial information on eye movements occurs via projections of the ADS into the frontal eye field (FEF; a premotor area that is responsible for guiding eye movements) located in the frontal lobe. This is demonstrated with anatomical tracing studies that reported of connections between areas CM-CL-IPS and the FEF,[29][30] and electro-physiological recordings that reported neural activity in both the IPS[31][32][33][30] and the FEF[34][35] prior to conducting saccadic eye-movements toward auditory targets.

Integration of locations with auditory objects[edit]

A surprising function of the ADS is with the discrimination and possible identification of sounds, which is commonly ascribed with the anterior STG and STS of the AVS. However, electrophysiological recordings from the posterior auditory cortex (areas CM-CL),[36][37] and IPS of monkeys,[38] as well a PET monkey study[39] reported of neurons that are selective to monkey vocalizations. One of these studies[37] also reported of neurons in areas CM-CL that are characterized with dual selectivity for both a vocalization and a sound location. A monkey study that recorded electrophysiological activity from neurons in the posterior insula also reported of neurons that discriminate monkey calls based on the identity of the speaker.[40] Similarly, human fMRI studies that instructed participants to discriminate voices reported an activation cluster in the pSTG.[41][42][43] A study that recorded activity from the auditory cortex of an epileptic patient further reported that the pSTG, but not aSTG, was selective for the presence of a new speaker.[44] A study that scanned fetuses in their third trimester of pregnancy with fMRI further reported of activation in area Spt when the hearing of voices was contrasted to pure tones.[45] The researchers also reported that a sub-region of area Spt was more selective to their mother's voice than unfamiliar female voices. This study thus suggests that the ADS is capable of identifying voices in addition to discriminating them.

The manner in which sound recognition in the pSTG-PT-Spt regions of the ADS differs from sound recognition in the anterior STG and STS of the AVS[41][46][47][48][49] was shown via electro-stimulation of an epileptic patient.[44] This study reported that electro-stimulation of the aSTG resulted in changes in the perceived pitch of voices (including the patient's own voice), whereas electro-stimulation of the pSTG resulted in reports that her voice was "drifting away." This report indicates a role for the pSTG in the integration of sound location with an individual voice. Consistent with this role of the ADS is a study that reported patients, with AVS damage but spared ADS (surgical removal of the anterior STG/MTG), were no longer capable of isolating environmental sounds in the contralesional space, whereas their ability of isolating and discriminating human voices remained intact.[50] Supporting a role for the pSTG-PT-Spt of the ADS with integrating auditory objects with sound locations are also studies that demonstrate a role for this region in the isolation of specific sounds. For example, two functional imaging studies correlated circumscribed pSTG-PT activation with the spreading of sounds into an increasing number of locations.[51][52] Accordingly, an fMRI study correlated the perception of acoustic cues that are necessary for separating musical sounds (pitch chroma) with pSTG-PT activation.[53]

Integration of phonemes with lip-movements[edit]

Although sound perception is primarily ascribed with the AVS, the ADS appears associated with several aspects of speech perception. For instance, in a meta-analysis of fMRI studies[54] in which the auditory perception of phonemes was contrasted with closely matching sounds, and the studies were rated for the required level of attention, the authors concluded that attention to phonemes correlates with strong activation in the pSTG-pSTS region. An intra-cortical recording study in which participants were instructed to identify syllables also correlated the hearing of each syllable with its own activation pattern in the pSTG.[55] Consistent with the role of the ADS in discriminating phonemes,[54] studies have ascribed the integration of phonemes and their corresponding lip movements (i.e., visemes) to the pSTS of the ADS. For example, an fMRI study[56] has correlated activation in the pSTS with the McGurk illusion (in which hearing the syllable "ba" while seeing the viseme "ga" results in the perception of the syllable "da"). Another study has found that using magnetic stimulation to interfere with processing in this area further disrupts the McGurk illusion.[57] The association of the pSTS with the audio-visual integration of speech has also been demonstrated in a study that presented participants with pictures of faces and spoken words of varying quality. The study reported that the pSTS selects for the combined increase of the clarity of faces and spoken words.[58] Corroborating evidence has been provided by an fMRI study[59] that contrasted the perception of audio-visual speech with audio-visual non-speech (pictures and sounds of tools). This study reported the detection of speech-selective compartments in the pSTS. In addition, an fMRI study[60] that contrasted congruent audio-visual speech with incongruent speech (pictures of still faces) reported pSTS activation. For a review presenting additional converging evidence regarding the role of the pSTS and ADS in phoneme-viseme integration see.[61]

Speech production[edit]

Studies of present-day humans have demonstrated a role for the ADS in speech production, particularly in the vocal expression of the names of objects. For instance, in a series of studies in which sub-cortical fibers were directly stimulated,[62] interference in the left pSTG and IPL resulted in errors during object-naming tasks, and interference in the left IFG resulted in speech arrest. Magnetic interference in the pSTG and IFG of healthy participants also produced speech errors and speech arrest, respectively[63] (Stewart et al., 2001; Acheson et al., 2011). One study has also reported that electrical stimulation of the left IPL caused patients to believe that they had spoken when they had not and that IFG stimulation caused patients to unconsciously move their lips.[64] The contribution of the ADS to the process of articulating the names of objects could to be dependent on the reception of afferents from the semantic lexicon of the AVS, as an intra-cortical recording study reported of activation in the posterior MTG prior to activation in the Spt-IPL region when patients named objects in pictures.[65] Intra-cortical electrical stimulation studies also reported that electrical interference to the posterior MTG was correlated with impaired object naming.[66][67]

Vocal mimicry[edit]

The involvement of the ADS in both speech perception and production has been further illuminated in several pioneering functional imaging studies that contrasted speech perception with overt or covert speech production.[68][69][70] These studies demonstrated that the pSTS is active only during the perception of speech, whereas area Spt is active during both the perception and production of speech. The authors concluded that the pSTS projects to area Spt, which converts the auditory input into articulatory movements.[71][72] Similar results have been obtained in a study in which participants' temporal and parietal lobes were electrically stimulated. This study reported that electrically stimulating the pSTG region interferes with sentence comprehension and that stimulation of the IPL interferes with the ability to vocalize the names of objects.[73] The authors also reported that stimulation in area Spt and the inferior IPL induced interference during both object-naming and speech-comprehension tasks. The role of the ADS in speech repetition is also congruent with the results of the other functional imaging studies that have localized activation during speech repetition tasks to ADS regions.[74][75][76] An intra-cortical recording study that recorded activity throughout most of the temporal, parietal and frontal lobes also reported activation in the pSTG, Spt, IPL and IFG when speech repetition is contrasted with speech perception.[77] Neuropsychological studies have also found that individuals with speech repetition deficits but preserved auditory comprehension (i.e., conduction aphasia) suffer from circumscribed damage to the Spt-IPL area.[78][79][80][81][82] or damage to the projections that emanate from this area and target the frontal lobe[83][84][85][86] Studies have also reported a transient speech repetition deficit in patients after direct intra-cortical electrical stimulation to this same region.[87][88][89] Insight into the purpose of speech repetition in the ADS is provided by longitudinal studies of children that correlated the learning of foreign vocabulary with the ability to repeat nonsense words.[90][91]

Speech monitoring[edit]

In addition to repeating and producing speech, the ADS appears to have a role in monitoring the quality of the speech output. Neuroanatomical evidence suggests that the ADS is equipped with descending connections from the IFG to the pSTG that relay information about motor activity (i.e., corollary discharges) in the vocal apparatus (mouth, tongue, vocal folds). This feedback marks the sound perceived during speech production as self-produced and can be used to adjust the vocal apparatus to increase the similarity between the perceived and emitted calls. Evidence for descending connections from the IFG to the pSTG has been offered by a study that electrically stimulated the IFG during surgical operations and reported the spread of activation to the pSTG-pSTS-Spt region.[92] A study[93] that compared the ability of aphasic patients with frontal, parietal or temporal lobe damage to quickly and repeatedly articulate a string of syllables reported that damage to the frontal lobe interfered with the articulation of both identical syllabic strings ("Bababa") and non-identical syllabic strings ("Badaga"), whereas patients with temporal or parietal lobe damage only exhibited impairment when articulating non-identical syllabic strings. Because the patients with temporal and parietal lobe damage were capable of repeating the syllabic string in the first task, their speech perception and production appears to be relatively preserved, and their deficit in the second task is therefore due to impaired monitoring. Demonstrating the role of the descending ADS connections in monitoring emitted calls, an fMRI study[94] instructed participants to speak under normal conditions or when hearing a modified version of their own voice (delayed first formant) and reported that hearing a distorted version of one's own voice results in increased activation in the pSTG. Further demonstrating that the ADS facilitates motor feedback during mimicry is an intra-cortical recording study[95] that contrasted speech perception and repetition. The authors reported that, in addition to activation in the IPL and IFG, speech repetition is characterized by stronger activation in the pSTG than during speech perception. For additional converging evidence regarding the role of the ADS in the relay of feedback motor connections from the vocal apparatus, see [96][97]

Analysis of intonations[edit]

Several studies demonstrated a role for the ADS in the perception and production of intonations. For instance, an fMRI study that instructed participants to rehearse speech, reported that perception of prosodic speech, when contrasted with flattened speech, results in a stronger activation of the PT-pSTG of both hemispheres.[98] In congruence, an fMRI study that compared the perception of hummed speech to natural speech didn't identify any brain area that is specific to humming, and thus concluded that humming is processed in the speech network.[99] fMRI studies[100][101] that instructed participants to analyze the rhythm of speech also reported of ADS activation (Spt, IPL, IFG). An fMRI study[102] that compared speech perception and production to the perception and production of humming noises, reported in both conditions that the overlaping activation area for perception and production (i.e., the area responsible for sensory-motor conversion) was located in area Spt of the ADS. Supporting evidence for the role of the ADS in the production of prosody are also studies.[103][104][105] reporting that patients diagnosed with apraxia of speech are additionally diagnosed with expressive dysprosody.

Phonological long-term memory[edit]

A growing body of evidence indicates that humans, in addition to having a long-term store for word meanings located in the MTG-TP of the AVS (i.e., the semantic lexicon), also have a long-term store for the names of objects located in the Spt-IPL region of the ADS (i.e., the phonological lexicon). For example, a study[106][107] examining patients with damage to the AVS (MTG damage) or damage to the ADS (IPL damage) reported that MTG damage results in individuals incorrectly identifying objects (e.g., calling a "goat" a "sheep," an example of semantic paraphasia). Conversely, IPL damage results in individuals correctly identifying the object but incorrectly pronouncing its name (e.g., saying "gof" instead of "goat," an example of phonemic paraphasia). Semantic paraphasia errors have also been reported in patients receiving intra-cortical electrical stimulation of the AVS (MTG), and phonemic paraphasia errors have been reported in patients whose ADS (pSTG, Spt, and IPL) received intra-cortical electrical stimulation.[73][108][109] Further supporting the role of the ADS in object naming is an MEG study that localized activity in the IPL during the learning and during the recall of object names.[110] A study that induced magnetic interference in participants' IPL while they answered questions about an object reported that the participants were capable of answering questions regarding the object's characteristics or perceptual attributes but were impaired when asked whether the word contained two or three syllables.[111] An MEG study has also correlated recovery from anomia (a disorder characterized by an impaired ability to name objects) with changes in IPL activation.[112] Further supporting the role of the IPL in encoding the sounds of words are studies reporting that, compared to monolinguals, bilinguals have greater cortical density in the IPL but not the MTG.[113][114] Because evidence shows that, in bilinguals, different phonological representations of the same word share the same semantic representation,[115] this increase in density in the IPL verifies the existence of the phonological lexicon: the semantic lexicon of bilinguals is expected to be similar in size to the semantic lexicon of monolinguals, whereas their phonological lexicon should be twice the size. Consistent with this finding, cortical density in the IPL of monolinguals also correlates with vocabulary size.[116][117] Notably, the functional dissociation of the AVS and ADS in object-naming tasks is supported by cumulative evidence from reading research showing that semantic errors are correlated with MTG impairment and phonemic errors with IPL impairment. Based on these associations, the semantic analysis of text has been linked to the inferior-temporal gyrus and MTG, and the phonological analysis of text has been linked to the pSTG-Spt- IPL[118][119][120]

Phonological working memory[edit]

Working memory is often treated as the temporary activation of the representations stored in long-term memory that are used for speech (phonological representations). This sharing of resources between working memory and speech is evident by the finding[121][122] that speaking during rehearsal results in a significant reduction in the number of items that can be recalled from working memory (articulatory suppression). The involvement of the phonological lexicon in working memory is also evidenced by the tendency of individuals to make more errors when recalling words from a recently learned list of phonologically similar words than from a list of phonologically dissimilar words (the phonological similarity effect).[121] Studies have also found that speech errors committed during reading are remarkably similar to speech errors made during the recall of recently learned, phonologically similar words from working memory.[123] Patients with IPL damage have also been observed to exhibit both speech production errors and impaired working memory[124][125][126][127] Finally, the view that verbal working memory is the result of temporarily activating phonological representations in the ADS is compatible with recent models describing working memory as the combination of maintaining representations in the mechanism of attention in parallel to temporarily activating representations in long-term memory.[122][128][129][130] It has been argued that the role of the ADS in the rehearsal of lists of words is the reason this pathway is active during sentence comprehension[131] For a review of the role of the ADS in working memory, see.[132]

Evolution of language[edit]

It is presently unknown why so many functions are ascribed to the human ADS. An attempt to unify these functions under a single framework was conducted in the 'From where to what' model of language evolution.[133][134] In accordance with this model, each function of the ADS indicates of a different intermediate phase in the evolution of language. The roles of sound localization and integration of sound location with voices and auditory objects is interpreted as evidence that the origin of speech is the exchange of contact calls (calls used to report location in cases of separation) between mothers and offspring. The role of the ADS in the perception and production of intonations is interpreted as evidence that speech began by modifying the contact calls with intonations, possibly for distinguishing alarm contact calls from safe contact calls. The role of the ADS in encoding the names of objects (phonological long-term memory) is interpreted as evidence of gradual transition from modifying calls with intonations to complete vocal control. The role of the ADS in the integration of lip movements with phonemes and in speech repetition is interpreted as evidence that spoken words were learned by infants mimicking their parents' vocalizations, initiailly by imitating their lip movements. The role of the ADS in phonological working memory is interpreted as evidence that the words learned through mimicry remained active in the ADS even when not spoken. This resulted with individuals capable of rehearsing a list of vocalizations, which enabled the production of words with several syllables. Further developments in the ADS enabled the rehearsal of lists of words, which provided the infra-structure for communicating with sentences.

See also[edit]

References[edit]

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