Primate auditory prototype in the evolution of the arcuate fasciculus

Balezeau, Fabien; Wilson, Benjamin; Gallardo, Guillermo; Dick, Frederic; Hopkins, William D.; Anwander, Alfred; Friederici, Angela D.; Griffiths, Timothy D.; Petkov, Christopher I.

doi:10.1038/s41593-020-0623-9

Cited by 71 publications

(73 citation statements)

References 30 publications

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“…The dorsal stream, which contains direct projections connecting posterior STG and lateral/inferior PFC (as well as indirect connections via posterior parietal cortex) in both species ( 27 ), harbors spatial as well as sensorimotor functions ( 17 ). On the basis of diffusion tensor imaging, it was found that the direct projection is denser and more left-lateralized in humans than in monkeys ( 66 , 67 ), but whether this quantitative difference can explain the qualitative difference in vocal production appears doubtful ( 68 ). Species differences in auditory–motor functions, including vocal behavior, are more likely to be found in the precise cross-stream coupling between ventral and dorsal streams ( 23 ).…”

Section: Discussionmentioning

confidence: 99%

Auditory representation of learned sound sequences in motor regions of the macaque brain

Archakov

DeWitt

Kuśmierek

et al. 2020

Proc. Natl. Acad. Sci. U.S.A.

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Human speech production requires the ability to couple motor actions with their auditory consequences. Nonhuman primates might not have speech because they lack this ability. To address this question, we trained macaques to perform an auditory–motor task producing sound sequences via hand presses on a newly designed device (“monkey piano”). Catch trials were interspersed to ascertain the monkeys were listening to the sounds they produced. Functional MRI was then used to map brain activity while the animals listened attentively to the sound sequences they had learned to produce and to two control sequences, which were either completely unfamiliar or familiar through passive exposure only. All sounds activated auditory midbrain and cortex, but listening to the sequences that were learned by self-production additionally activated the putamen and the hand and arm regions of motor cortex. These results indicate that, in principle, monkeys are capable of forming internal models linking sound perception and production in motor regions of the brain, so this ability is not special to speech in humans. However, the coupling of sounds and actions in nonhuman primates (and the availability of an internal model supporting it) seems not to extend to the upper vocal tract, that is, the supralaryngeal articulators, which are key for the production of speech sounds in humans. The origin of speech may have required the evolution of a “command apparatus” similar to the control of the hand, which was crucial for the evolution of tool use.

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Section: Discussionmentioning

confidence: 99%

Auditory representation of learned sound sequences in motor regions of the macaque brain

Archakov

DeWitt

Kuśmierek

et al. 2020

Proc. Natl. Acad. Sci. U.S.A.

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“…If categorisation is emergent in non-human primates and ubiquitous among modern humans, then parsimony points to the evolution of symbol use-and language-long before Homo sapiens. Pedersen (2012) concludes, following a study of the ability of captive bonobos to acquire visual and auditory symbols, that language evolved from deep-rooted semantic and conceptual abilities in the last common ancestor of chimpanzees and hominins, some six million years ago, and in recent work, it is argued that the neural, auditory pathway for language evolved at least 25 million years ago among monkeys (Balezeau et al 2020). The shared inheritance is based on biological and cognitive similarities in how humans and apes experience the world through their bodies and senses (Lakoff and Johnson 1999).…”

Section: Conventions and Categories Among Non-human Primatesmentioning

confidence: 99%

Semiotics and the Origin of Language in the Lower Palaeolithic

Barham

Everett

2020

J Archaeol Method Theory

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This paper argues that the origins of language can be detected one million years ago, if not earlier, in the archaeological record of Homo erectus. This controversial claim is based on a broad theoretical and evidential foundation with language defined as communication based on symbols rather than grammar. Peirce's theory of signs (semiotics) underpins our analysis with its progression of signs (icon, index and symbol) used to identify artefact forms operating at the level of symbols. We draw on generalisations about the multiple social roles of technology in pre-industrial societies and on the contexts tool-use among non-human primates to argue for a deep evolutionary foundation for hominin symbol use. We conclude that symbol-based language is expressed materially in arbitrary social conventions that permeate the technologies of Homo erectus and its descendants, and in the extended planning involved in the caching of tools and in the early settlement of island Southeast Asia.

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“…Human area 44 is interconnected with areas caudal to auditory cortex via the dorsal arcuate fasciculus pathway 13 . A recent comparative study showed a homolog of this dorsal auditory pathway in macaques 8 projecting from caudo-medial regions near to those that we electrically stimulated, which elicited vlPFC activity.…”

Section: Discussionmentioning

confidence: 68%

“…Left hemisphere areas posterior to Heschl’s gyrus (HG; an anatomical landmark associated with primary auditory cortex) are interconnected with Brodmann areas 44 and 45 in vlPFC by way of the dorsal arcuate fasciculus pathway 13 . There is now evidence for an auditory homolog in chimpanzees and macaques, with its left hemisphere lateralization as a prominent human-specific difference 8 . In monkeys, vlPFC neurons respond to vocalization sounds 14 , and single neuron tractography has shown evidence for directional connectivity between non-primary auditory (lateral belt) areas and vlPFC 15 .…”

Section: Introductionmentioning

confidence: 99%

Common Fronto-temporal Effective Connectivity in Humans and Monkeys

Rocchi

Oya

Balezeau

et al. 2020

Preprint

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Highlights 22 • Privileged human auditory to inferior frontal connectivity, linked to monkeys 23 • Common auditory to parahippocampal effective connectivity in both species 24 • Greater lateralization in human effective connectivity, more symmetrical in monkeys 25 • Human fronto-temporal network function rooted in evolutionarily conserved signature 26 27 eTOC short summary 28 Functional connectivity between regions crucial for language and declarative memory is thought to 29 have substantially differentiated in humans. Using a new technique to similarly visualize directional 30 effective connectivity in humans and monkeys, we found remarkably comparable connectivity patterns 31 in both species between fronto-temporal regions crucial for cognition. 32 33 ABSTRACT 36 Cognitive pathways supporting human language and declarative memory are thought to have uniquely 37 evolutionarily differentiated in our species. However, cross-species comparisons are missing on site-38 specific effective connectivity between regions important for cognition. We harnessed a new approach 39 using functional imaging to visualize the impact of direct electrical brain stimulation in human 40 neurosurgery patients. Applying the same approach with macaque monkeys, we found remarkably 41 comparable patterns of effective connectivity between auditory cortex and ventro-lateral prefrontal 42 cortex (vlPFC) and parahippocampal cortex in both species. Moreover, in humans electrical 43 tractography revealed rapid evoked potentials in vlPFC from stimulating auditory cortex and speech 44 sounds drove vlPFC, consistent with prior evidence in monkeys of direct projections from auditory 45 cortex to vocalization responsive regions in vlPFC. The results identify a common effective 46 connectivity signature that from auditory cortex is equally direct to vlPFC and indirect to the homology, convergence or divergence, can be of substantial theoretical significance: Within the motor 52 domain, human and nonhuman primates have direct cortico-spinal projections subserving fine 53 movement control that are indirect in rodents 1 . Also, human laryngeal motor cortex projects directly to 54 a brain stem nucleus (ambiguus) controlling laryngeal muscles 2 . Such projections for vocal production 55 are more indirect in nonhuman primates 3 and rodents 4 , shedding light on human speech evolution 5 . 56 Language defines us as a species and because of its prominent role in declarative memory 57 substantial evolutionary differentiation of human cognitive pathways is expected. Comparative studies 58 often see considerable levels of evolutionary conservation alongside insights on species-specific 59 differences 6-12 . Yet, certain cross-species comparisons are missing, such as on the impact of directed 60 effective connectivity with the required precision of site-specific perturbation that can be applied to 61 both human and nonhuman primates. Thereby, the question on the extent of differentiation versus 62 conservation in primate fronto-temporal systems-although crucial fo...

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Primate auditory prototype in the evolution of the arcuate fasciculus

Cited by 71 publications

References 30 publications

Auditory representation of learned sound sequences in motor regions of the macaque brain

Auditory representation of learned sound sequences in motor regions of the macaque brain

Semiotics and the Origin of Language in the Lower Palaeolithic

Common Fronto-temporal Effective Connectivity in Humans and Monkeys

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