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Auditory ventral 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. Material was copied from this source, which is available under a Creative Commons Attribution 4.0 International License.

The auditory ventral stream (AVS) is a neuroanatomical pathway in the primate’s brain that connects the primary auditory cortex with the middle temporal gyrus/temporal pole and the inferior frontal gyrus. The primary function of this pathway is sound recognition. A common moniker for this neuroanatomical pathway is the auditory ‘what’ pathway.

History of neurolinguistics[edit]

Throughout the 20th century, our knowledge of language processing in the brain was dominated by the Wernicke-Lichtheim-Geschwind model.[1][2][3] This model is primarily based on research conducted on brain-damaged individuals who were reported to possess a variety of language related disorders. In accordance with this model, words are perceived via a specialized word reception center (Wernicke’s area) that is located in the left temporoparietal junction. This region then projects to a word production center (Broca’s area) that is located in the left inferior frontal gyrus. Because almost all language input was thought to funnel via Wernicke’s area and all language output to funnel via Broca’s area, it became extremely difficult to identify the basic properties of each region. This lack of clear definition for the contribution of Wernicke’s and Broca’s regions to human language rendered it extremely difficult to identify their homologues in other primates.[4] With the advent of the MRI and its application for lesion mappings, however, it was shown that this model is based on incorrect correlations between symptoms and lesions.[5][6][7][8][9][10][11] The refutation of such an influential and dominant model opened the door to new models of language processing in the brain.

Anatomy of the auditory ventral and dorsal streams[edit]

In the last two decades, significant advances occurred in our understanding of the neural processing of sounds in primates. Initially by recording of neural activity in the auditory cortices of monkeys[12][13] and later elaborated via histological staining[14][15][16] and fMRI scanning studies,[17] 3 auditory fields were identified in the primary auditory cortex, and 9 associative auditory fields were shown to surround them (Figure 1 top left). Anatomical tracing and lesion studies further indicated of a separation between the anterior and posterior auditory fields, with the anterior primary auditory fields (areas R-RT) projecting to the anterior associative auditory fields (areas AL-RTL), and the posterior primary auditory field (area A1) projecting to the posterior associative auditory fields (areas CL-CM).[18][19][20][21] Recently, evidence accumulated that indicates homology between the human and monkey auditory fields. In humans, histological staining studies revealed two separate auditory fields in the primary auditory region of Heschl’s gyrus,[22][23] and by mapping the tonotopic organization of the human primary auditory fields with high resolution fMRI and comparing it to the tonotopic organization of the monkey primary auditory fields, homology was established between the human anterior primary auditory field and monkey area R (denoted in humans as area hR) and the human posterior primary auditory field and the monkey area A1 (denoted in humans as area hA1).[24][25][26][27][28] Intra-cortical recordings from the human auditory cortex further demonstrated similar patterns of connectivity to the auditory cortex of the monkey. Recording from the surface of the auditory cortex (supra-temporal plane) reported that the anterior Heschl’s gyrus (area hR) projects primarily to the middle-anterior superior temporal gyrus (mSTG-aSTG) and the posterior Heschl’s gyrus (area hA1) projects primarily to the posterior superior temporal gyrus (pSTG) and the planum temporale (area PT; Figure 1 top right).[29][30] Consistent with connections from area hR to the aSTG and hA1 to the pSTG is an fMRI study of a patient with impaired sound recognition (auditory agnosia), who was shown with reduced bilateral activation in areas hR and aSTG but with spared activation in the mSTG-pSTG.[31] This connectivity pattern is also corroborated by a study that recorded activation from the lateral surface of the auditory cortex and reported of simultaneous non-overlapping activation clusters in the pSTG and mSTG-aSTG while listening to sounds.[32]

Downstream to the auditory cortex, anatomical tracing studies in monkeys delineated projections from the anterior associative auditory fields (areas AL-RTL) to ventral prefrontal and premotor cortices in the inferior frontal gyrus (IFG)[33][34] and amygdala.[35] Cortical recording and functional imaging studies in macaque monkeys further elaborated on this processing stream by showing that acoustic information flows from the anterior auditory cortex to the temporal pole (TP) and then to the IFG.[36][37][38][39][40][41] This pathway is commonly referred to as the auditory ventral stream (AVS; Figure 1, bottom left-red arrows). In contrast to the anterior auditory fields, tracing studies reported that the posterior auditory fields (areas CL-CM) project primarily to dorsolateral prefrontal and premotor cortices (although some projections do terminate in the IFG.[42][34] Cortical recordings and anatomical tracing studies in monkeys further provided evidence that this processing stream flows from the posterior auditory fields to the frontal lobe via a relay station in the intra-parietal sulcus (IPS).[43][44][45][46][47][48] This pathway is commonly referred to as the auditory dorsal stream (ADS; Figure 1, bottom left-blue arrows). Comparing the white matter pathways involved in communication in humans and monkeys with diffusion tensor imaging techniques indicates of similar connections of the AVS and ADS in the two species (Monkey,[47] Human[49][50][51][52][53][54]). In humans, the pSTG was shown to project to the parietal lobe (sylvian parietal-temporal junction- inferior parietal lobule; Spt-IPL), and from there to dorsolateral prefrontal and premotor cortices (Figure 1, bottom right-blue arrows), and the aSTG was shown to project to the anterior temporal lobe (middle temporal gyrus-temporal pole; MTG-TP) and from there to the IFG (Figure 1 bottom right-red arrows).

Auditory ventral stream[edit]

Sound Recognition[edit]

Accumulative converging evidence indicates that the AVS is involved in recognizing auditory objects. At the level of the primary auditory cortex, recordings from monkeys showed higher percentage of neurons selective for learned melodic sequences in area R than area A1,[55] and a study in humans demonstrated more selectivity for heard syllables in the anterior Heschl’s gyrus (area hR) than posterior Heshcl’s gyrus (area hA1).[56] In downstream associative auditory fields, studies from both monkeys and humans reported that the border between the anterior and posterior auditory fields (Figure 1-area PC in the monkey and mSTG in the human) processes pitch attributes that are necessary for the recognition of auditory objects.[57] The anterior auditory fields of monkeys were also demonstrated with selectivity for con-specific vocalizations with intra-cortical recordings.[58][59][60] and functional imaging[61][37][62] One fMRI monkey study further demonstrated a role of the aSTG in the recognition of individual voices.[37] The role of the human mSTG-aSTG in sound recognition was demonstrated via functional imaging studies that correlated activity in this region with isolation of auditory objects from background noise,[63][64] and with the recognition of spoken words,[65][66][67][68][69][70][71] voices,[72] melodies,[73][74] environmental sounds,[75][76][77] and non-speech communicative sounds.[78] A Meta-analysis of fMRI studies[79] further demonstrated functional dissociation between the left mSTG and aSTG, with the former processing short speech units (phonemes) and the latter processing longer units (e.g., words, environmental sounds). A study that recorded neural activity directly from the left pSTG and aSTG reported that the aSTG, but not pSTG, was more active when the patient listened to speech in her native language than unfamiliar foreign language.[80] Consistently, electro stimulation to the aSTG of this patient resulted in impaired speech perception[80] (see also[81][82] for similar results). Intra-cortical recordings from the right and left aSTG further demonstrated that speech is processed laterally to music.[80] An fMRI study of a patient with impaired sound recognition (auditory agnosia) due to brainstem damage was also shown with reduced activation in areas hR and aSTG of both hemispheres when hearing spoken words and environmental sounds.[31] Recordings from the anterior auditory cortex of monkeys while maintaining learned sounds in working memory,[83] and the debilitating effect of induced lesions to this region on working memory recall,[84][85][86] further implicate the AVS in maintaining the perceived auditory objects in working memory. In humans, area mSTG-aSTG was also reported active during rehearsal of heard syllables with MEG.[87] and fMRI[88] The latter study further demonstrated that working memory in the AVS is for the acoustic properties of spoken words and that it is independent to working memory in the ADS, which mediates inner speech. Working memory studies in monkeys also suggest that in monkeys, in contrast to humans, the AVS is the dominant working memory store.[89]

In humans, downstream to the aSTG, the MTG and TP are thought to constitute the semantic lexicon, which is a long-term memory repository of audio-visual representations that are interconnected on the basis of semantic relationships. (See also the reviews by[90][91] discussing this topic). The primary evidence for this role of the MTG-TP is that patients with damage to this region (e.g., patients with semantic dementia or herpes simplex virus encephalitis) are reported[92][93] with an impaired ability to describe visual and auditory objects and a tendency to commit semantic errors when naming objects (i.e., semantic paraphasia). Semantic paraphasias were also expressed by aphasic patients with left MTG-TP damage[94][95] and were shown to occur in non-aphasic patients after electro-stimulation to this region.[96][97] or the underlying white matter pathway[98] Two meta-analyses of the fMRI literature also reported that the anterior MTG and TP were consistently active during semantic analysis of speech and text;[99][100] and an intra-cortical recording study correlated neural discharge in the MTG with the comprehension of intelligible sentences.[101]

Sentence comprehension[edit]

In addition to extracting meaning from sounds, the MTG-TP region of the AVS appears to have a role in sentence comprehension, possibly by merging concepts together (e.g., merging the concept 'blue' and 'shirt to create the concept of a 'blue shirt'). The role of the MTG in extracting meaning from sentences has been demonstrated in functional imaging studies reporting stronger activation in the anterior MTG when proper sentences are contrasted with lists of words, sentences in a foreign or nonsense language, scrambled sentences, sentences with semantic or syntactic violations and sentence-like sequences of environmental sounds.[102][103][104][105][106][107][108][109] One fMRI study[110] in which participants were instructed to read a story further correlated activity in the anterior MTG with the amount of semantic and syntactic content each sentence contained. An EEG study[111] that contrasted cortical activity while reading sentences with and without syntactic violations in healthy participants and patients with MTG-TP damage, concluded that the MTG-TP in both hemispheres participate in the automatic (rule based) stage of syntactic analysis (ELAN component), and that the left MTG-TP is also involved in a later controlled stage of syntax analysis (P600 component). Patients with damage to the MTG-TP region have also been reported with impaired sentence comprehension.[112][113][114] See review[115] for more information on this topic.

Bilaterality[edit]

In contradiction to the Wernicke-Lichtheim-Geschwind model that implicates sound recognition to occur solely in the left hemisphere, studies that examined the properties of the right or left hemisphere in isolation via unilateral hemispheric anesthesia (i.e., the WADA procedure[116]) or intra-cortical recordings from each hemisphere[101] provided evidence that sound recognition is processed bilaterally. Moreover, a study that instructed patients with disconnected hemispheres (i.e., split-brain patients) to match spoken words to written words presented to the right or left hemifields, reported vocabulary in the right hemisphere that almost matches in size with the left hemisphere[117] (The right hemisphere vocabulary was equivalent to the vocabulary of a healthy 11-years old child). This bilateral recognition of sounds is also consistent with the finding that unilateral lesion to the auditory cortex rarely results in deficit to auditory comprehension (i.e., auditory agnosia), whereas a second lesion to the remaining hemisphere (which could occur years later) does.[118][119] Finally, as mentioned earlier, an fMRI scan of an auditory agnosia patient demonstrated bilateral reduced activation in the anterior auditory cortices,[31] and bilateral electro-stimulation to these regions in both hemispheres resulted with impaired speech recognition.[80]

See also[edit]

References[edit]

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