Origins of Language: Constraints on Hypotheses

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Thus, the biological explanation of the lack of complex vocal learning in non-human primates must have something to do with brain structure. Kuypers explored the connections from motor cortex to subcortical motor systems in the brainstem and spinal cord, and compared these between cats, non-human primates chimpanzees and macaques , and humans. He examined in particular the motor neurons controlling laryngeal muscles, located in the nucleus ambiguus of the medulla.

He found that there were projections from cortical motor neurons directly onto these motor neurons only in humans. In cats or non-human primates, only multi-synaptic indirect connections were present to ambigual motor neurons. Interestingly, Kuypers found that chimpanzees and macaques do have direct connections to brainstem nuclei controlling the face lips and jaw , while cats lack these. This argument is consistent with lesion data: while lesions to motor cortex can induce long-lasting mutism in humans, matched lesions have no effect upon vocal production in monkeys Sutton et al.

Lesions to lateral cortex often severely disrupt human speech, but spare innate species-typical vocalizations like laughter and crying Foerster, ; Groswasser et al. All that is missing in chimpanzees is laryngeal control. These data, and other convergent data from birds see below , has led many comparative neuroscientists to endorse the idea that direct cortico-motor connections to the larynx play a key role in human speech abilities e.

How did humans develop direct connections that are lacking in other primates? The cortico-spinal tract is a major descending pathway from motor cortex down to motor neurons within the spinal cord. Cortico-spinal axons originate in pyramidal neurons in layer V of the neocortex, mostly in primary motor cortex but also from premotor cortex, the supplementary motor area SMA , cingulate gyrus, and somatosensory cortex.

A clear homolog of the cortico-spinal tract is present in all mammals. A closely related set of cortico-motor projections make up the cortico-bulbar tract, which project from cortex down to various brainstem motor nuclei found in the trigeminal CN V, controlling the jaw , facial CN VII: lips and other facial musculature , and hypoglossal CN XII, controlling the tongue nuclei. Thus, in primates, the cortico-bulbar and cortico-spinal tracts together innervate motor neurons above and below the key laryngeal motor neurons located in the nucleus ambiguus CN X, containing the motor neurons of the vagus nerve complex, including the superior and recurrent laryngeal nerves.

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I suggest that either, or both, of these tracts provided a precursor of the direct cortico-ambigual connections found in humans. Why do such direct connections develop in humans but not other primates? An intriguing hypothesis has been put forward by Terrence Deacon, involving competition between an innate call system based in the brainstem, and the cortico-motor system.

This system can produce the entire species-typical vocal repertoire of cats or squirrel monkeys, or innate vocalizations like laughter and crying in humans, and does not rely upon cortical input hence, anencephalic human babies who lack a neocortex can still smile, laugh, and cry normally. Deacon has suggested that, during development, there is competition between this prepotent brainstem system and cortical axons projecting down through the brainstem, which transiently connect to laryngeal motor neurons in the nucleus ambiguus, but are out-competed by the innate vocal system projections from PAG and other centers Deacon, , This hypothesis has various testable predictions, and even suggests that direct cortico-motor connections could be elicited experimentally in other mammals, if the innate call system was reduced by lesions at the right stage of development along the lines of Roe et al.

However, this aspect of speech does provide a simple, clear example of how a particular neural circuit involved in spoken language might have evolved via exaptation of a pre-existing motor circuit found in other primates. However, it is clearly both testable, and consistent with a considerable body of knowledge from comparative neuroscience.

This idea was over extended by Lichtheim and Geschwind to include a third hypothetical association area in the angular gyrus. For a detailed history of this discussion see Catani and Mesulam, The advent of DTI and in vivo tractography has breathed considerable new life into these old ideas, documenting differences between human brains and those of other primates Rilling et al. As in the previous example, there appear to be significant differences among species in the intracortical white-matter connections between temporal, parietal, and frontal regions that are plausibly related to speech motor control see Petkov and Jarvis, this issue.

In particular, Rilling and colleagues found that while the macaque homolog of the arcuate fasciculus makes only specific and limited connections between the superior temporal gyrus and regions of the lateral prefrontal cortex, the human arcuate makes rich and extensive connections to the middle and inferior temporal gyri as well. This expansion of the connectivity from prefrontal regions to essentially the entire temporal lobe may be linked to a relative expansion in humans of both frontal Deacon, ; Schoenemann et al.

This expanded connectivity was also found, but to a limited degree, in one of the four chimpanzee brains scanned. The expansion and elaboration of the arcuate fasciculus in humans has a more interesting implication in the context of the current topic of exaptation, because many have noted that this pathway is involved not only in speech imitation but also in some aspects of syntax processing.

Although Broca himself viewed his eponymous area as primarily involved in speech output, it has become abundantly clear that premotor areas such as BA 44 are also involved in auditory comprehension, and syntax processing in particular e. Because this issue is more thoroughly reviewed elsewhere in this issue, I will not go into the details here. The logic underlying this suggestion is similar to that underlying the motor theory of speech production Liberman et al.

The prefrontal component of this system is, at birth, concerned basically with motor control. It develops, through babbling and later practice with speech production, a quite complex repertoire of automatized vocal actions. This initially occurs with auditory guidance, but has little significance for auditory comprehension itself. However, once such a learned cortical repertoire exists, it could provide a useful, highly articulated basis for auditory phonetic comprehension knowing what a sound is based on the actions that would be needed to produce it and, at a higher level, syntactic, or semantic knowing what a sentence means based on the structures that would be needed to generate that meaning.

As phrased above, this hypothesis could apply either to ontogeny during individual brain development or phylogeny during the evolution of the required neural circuits in the species. However, one reason to doubt a purely ontogenetic interpretation of syntactic circuitry is provided by studies of signed language Bellugi et al. This suggests that the appropriate connections develop reliably in all humans, regardless of linguistic modality, and thus suggests an influence of an evolved pattern of connectivity in addition to the role of cortical plasticity during individual development.

Exaptive hypothesis 2 thus suggests that the intracortical connections of the human arcuate fasciculus initially evolved for the specific purpose of vocal imitation. These connections, once in place, were then again exapted for use in the more complex task of syntactic comprehension, and particularly between premotor control regions and posterior regions involved in semantic interpretation. This exaptation would have constituted a second evolutionary event, occurring afterward and perhaps for different selective reasons from the first.

The third exaptive hypothesis considered here is closely related to the previous one, and concerns the evolution of specific cortical regions involved in syntax. While the previous hypothesis is hodological, concerned with connections, this one is cytoarchitectonic, and concerned with the computational specializations of specific cortical regions. This hypothesis builds largely upon the work of Angela Friederici and her colleagues Friederici et al. Four core regions can be distinguished, the first three designated by their BA:.

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In an important study, Horwitz et al. They found that BA 44 was activated not only during speech or sign production, but also during complex, volitional movements of the limbs or vocal apparatus with no linguistic content. In contrast, BA 45 was activated only during the production of either spoken or signed language complex narratives, so including phonological, syntactic, and semantic components.

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In both cases, activations were significantly above baseline only in the left hemisphere. Cytoarchitectonically, each of the four regions above is distinct in terms of the granularity of layer 4 of neocortex. Connectivity also varies among these regions. BA 45B is heavily connected to eye movement circuitry such as the frontal and supplementary eye fields.

While BA 45A also makes extensive frontal connections, it is unique in having strong connections to superior temporal and auditory areas Gerbella et al. Many theorists have suggested that the hierarchical nature of linguistic structures is related in some way to the hierarchical nature of motor planning e. A second and not mutually exclusive hypothesis has not, to my knowledge, been previously suggested.

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Apes and Old World primates like chimpanzees and macaques have binocular vision and trichromacy, reflecting an increased importance of the visual modality relative to sound and olfaction. For review of the importance of gaze and visual cueing in the evolution of cognition and language see Fitch et al. While the movement of the eyes is clearly a motor function, its control requires strong intracortical communication from visual and multi-modal areas.

When such visual dependency is combined with intense social pressures, we might expect the computation of eye movements to have a more abstract and generalized component than limb or hand movements. Since, in the macaque, one portion of BA 45 is closely linked to eye movements, while the other makes long-distance cortical connections, I suggest that the abstract and amodal computations involved in language whether spoken or signed had a pre-adaptive foundation in the social and visually guided aspects of gaze that are, by hypothesis, subserved by BA 45B.

These two hypotheses may in fact be complementary, in the sense that the special role of BA 44 in language production and processing may represent a kind of fusion of the two flanking regions, specifically the hierarchical premotor functions of BA 6, and the multi-modal, integrative, and social functions of BA The result would be a more abstract computational process than hierarchical motor planning: an operator that can combine or unify pre-existing conceptual units motor actions, vocalizations, or visual objects to freely create a discrete infinity of modality-independent cognitive structures.

Hagoort, b. Whether during comprehension or in production, such an operator must quickly retrieve items from memory e. Could hierarchy-building circuitry in BA 6 and the deep frontal operculum, evolved in the context of motor planning and dedicated to motor control, be exapted to produce a general purpose, amodal, two-way circuit that can perform the computational equivalent of Merge or Unify?

While this hypothesis clearly remains speculative at present, it has several points to recommend it:. Studies of macaque mirror neurons and the human mirror system provide a plausible foundation for the two-way nature of this system, building on a pre-existing mirror system for interpreting the actions of others;. Not only is this exaptive hypothesis consistent with the data above, but it makes several specific testable predictions about the structure, connectivity, and function of BA BA 45 in humans should be more amodal than other components of the LIFG, and in particular its white-matter connections should be longer, and fan out more widely, than those of other regions;.

Anatomically, the cytoarchitecture of BA 45 should be less motor-driven, more perceptually embedded, and thus more suited to amodal cognition than BA 6 or BA 44 as already suggested by its granular layer 4 ;. In monkeys, cells in BA 45A should fire in a much wider variety of situations than BA 44 or BA 6 including in particular social cognition tasks. I see such hypotheses, when built upon a solid foundation of comparative neuroscientific data, as presenting numerous testable predictions and avenues for profitable empirical investigation. I will end with a brief attempt to clarify the role of comparative research in testing evolutionary hypotheses in general, and exaptive hypotheses in particular.

In brief, we can use comparison of homologous traits in closely related species to derive inferences about ancestral states. Convergent evolution plays a central role in testing evolutionary hypotheses, because each example of a convergently evolved trait represents an independent evolutionary event, and thus an independent data point for statistical testing Harvey and Pagel, ; Pagel, In contrast, a trait that is homologous among a group of species has, by definition, evolved only once in that clade, and even if there are hundreds of species sharing the trait, they constitute only a single independent data point.

The clade used most frequently in comparative tests regarding language evolution are birds, Class Aves, which have evolved numerous traits convergently with some mammals e. A homologous trait is one that is shared among a group of related organisms by virtue of its presence in their common ancestor. When attempting to build a phylogeny, systematists distinguish between two classes of homology. Feathers are a synapomorphy among living bird species all birds have them, and all living non-birds lack them , while the possession of a heart or a mouth are symplesiomorphies all birds have them, but so do all other vertebrates.

However, in the current context we are concerned with rebuilding ancestral states, however far back they might go, and so we will discuss homology in general. Homology is a relative concept: it depends on what trait is being examined, and what particular clade is being discussed. Thus, for example, the wings of birds and bats are homologous as forelimbs because they both derive from the forelimb of the shared tetrapod ancestor of birds and mammals but are convergently evolved analogs as wings. Furthermore, correct determination of homology depends upon the level of mechanistic detail being discussed.

The complex, image-forming eyes found in insects, octopus, or vertebrates evolved convergently Allman, but their location is nonetheless controlled by a homologous transcription factor Pax-6 Quiring et al. Such a situation has been termed deep homology and appears to play a surprisingly important role in human evolution cf. Carroll, ; Fitch, ; Shubin et al. Careful examination of homologous traits in multiple species allows us to reconstruct traits that were present in the common ancestor of those species.

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For example, the corpus callosum is found in all placental mammals eutherians , but is absent in marsupials and monotremes. This allows us to conclude that the corpus callosum was not present in the common ancestor of all mammals, but arose in the LCA of living eutherians. In contrast, the anterior commissure is found in marsupials, and more widely among vertebrates including birds, suggesting that it evolved rather early in tetrapods. Such inferences about ancestral states depend on solid comparative neuroanatomy in living organisms, and no fossil evidence is required to roughly date such evolutionary events.

A broad comparative analysis is also important to determine the directionality of any evolutionary changes in different lineages.

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It is important to note that traits can be lost as well as gained in evolution. There is no way to know, based on a simple comparison of two species that differ in some trait, what the directionality of change might have been, and this requires outgroup comparisons with other related species. For example, one might think that the sexual swellings surrounding the vaginal area in female chimpanzees are a primitive feature of primates, given that such swellings are also seen in macaques and baboons.

Origins of Language: Constraints on Hypotheses Origins of Language: Constraints on Hypotheses
Origins of Language: Constraints on Hypotheses Origins of Language: Constraints on Hypotheses
Origins of Language: Constraints on Hypotheses Origins of Language: Constraints on Hypotheses
Origins of Language: Constraints on Hypotheses Origins of Language: Constraints on Hypotheses
Origins of Language: Constraints on Hypotheses Origins of Language: Constraints on Hypotheses
Origins of Language: Constraints on Hypotheses Origins of Language: Constraints on Hypotheses
Origins of Language: Constraints on Hypotheses Origins of Language: Constraints on Hypotheses
Origins of Language: Constraints on Hypotheses Origins of Language: Constraints on Hypotheses
Origins of Language: Constraints on Hypotheses

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