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Understanding in an instant: neurophysiological evidence for mechanistic language circuits in the brain.

Pulvermüller F, Shtyrov Y, Hauk O - Brain Lang (2009)

Bottom Line: A key concept is that of discrete distributed cortical circuits with specific inter-area topographies.The full activation, or ignition, of specifically distributed binding circuits explains the near-simultaneity of early neurophysiological indexes of lexical, syntactic and semantic processing.Activity spreading within circuits determined by between-area conduction delays accounts for comprehension-related regional activation differences in the millisecond range.

View Article: PubMed Central - PubMed

Affiliation: Medical Research Council, Cognition and Brain Sciences Unit, 15 Chaucer Road, Cambridge, UK. friedemann.pulvermuller@mrc-cbu.cam.ac.uk

ABSTRACT
How long does it take the human mind to grasp the idea when hearing or reading a sentence? Neurophysiological methods looking directly at the time course of brain activity indexes of comprehension are critical for finding the answer to this question. As the dominant cognitive approaches, models of serial/cascaded and parallel processing, make conflicting predictions on the time course of psycholinguistic information access, they can be tested using neurophysiological brain activation recorded in MEG and EEG experiments. Seriality and cascading of lexical, semantic and syntactic processes receives support from late (latency approximately 1/2s) sequential neurophysiological responses, especially N400 and P600. However, parallelism is substantiated by early near-simultaneous brain indexes of a range of psycholinguistic processes, up to the level of semantic access and context integration, emerging already 100-250ms after critical stimulus information is present. Crucially, however, there are reliable latency differences of 20-50ms between early cortical area activations reflecting lexical, semantic and syntactic processes, which are left unexplained by current serial and parallel brain models of language. We here offer a mechanistic model grounded in cortical nerve cell circuits that builds upon neuroanatomical and neurophysiological knowledge and explains both near-simultaneous activations and fine-grained delays. A key concept is that of discrete distributed cortical circuits with specific inter-area topographies. The full activation, or ignition, of specifically distributed binding circuits explains the near-simultaneity of early neurophysiological indexes of lexical, syntactic and semantic processing. Activity spreading within circuits determined by between-area conduction delays accounts for comprehension-related regional activation differences in the millisecond range.

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Lexical and semantic representations modelled at the mechanistic level of cortical circuits. As word learning implies linking spoken word forms to their respective articulatory patterns, the abstract articulatory acoustic pattern of a spoken word form is stored by strongly connected lexical circuits distributed over superior-temporal and inferior-frontal cortex (perisylvian cell assembly, a) In literate speakers, information about writing gestures and written word forms are bound to spoken word form representations; this binding of knowledge is cortically grounded in a halo of perisylvian cell assemblies extending into hand-related motor and premotor areas and fusiform gyrus (b). Meaningful words bind, in an arbitrary manner, information about their form and the concepts they refer to. Abstract semantic links are realized by the multiple connections between perisylvian cell assemblies and modality-specific semantic circuits in various parts of the cortex, for example in anterior- and inferior-temporal cortex (animal and color concepts, c), posterior-inferior and middle temporal cortex (tools and shapes, d), inferior-frontal cortex (face and articulatory actions, e), dorso-lateral fronto-central cortex (arm actions, f), and dorsal central cortex (leg actions, g). Ignition of these networks upon stimulation accounts for early near-simultaneity of neurocognitive indexes of psycholinguistic information access and conduction delays through long-distance cortico-cortical connections within these circuits explain fine-grained activation delays.
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fig5: Lexical and semantic representations modelled at the mechanistic level of cortical circuits. As word learning implies linking spoken word forms to their respective articulatory patterns, the abstract articulatory acoustic pattern of a spoken word form is stored by strongly connected lexical circuits distributed over superior-temporal and inferior-frontal cortex (perisylvian cell assembly, a) In literate speakers, information about writing gestures and written word forms are bound to spoken word form representations; this binding of knowledge is cortically grounded in a halo of perisylvian cell assemblies extending into hand-related motor and premotor areas and fusiform gyrus (b). Meaningful words bind, in an arbitrary manner, information about their form and the concepts they refer to. Abstract semantic links are realized by the multiple connections between perisylvian cell assemblies and modality-specific semantic circuits in various parts of the cortex, for example in anterior- and inferior-temporal cortex (animal and color concepts, c), posterior-inferior and middle temporal cortex (tools and shapes, d), inferior-frontal cortex (face and articulatory actions, e), dorso-lateral fronto-central cortex (arm actions, f), and dorsal central cortex (leg actions, g). Ignition of these networks upon stimulation accounts for early near-simultaneity of neurocognitive indexes of psycholinguistic information access and conduction delays through long-distance cortico-cortical connections within these circuits explain fine-grained activation delays.

Mentions: Neuronal circuits processing spoken word forms comprise neurons in superior-temporal cortex activated by phonetic features of a spoken word, neurons in inferior-frontal cortex programming and controlling articulatory movements and additional neurons connecting the acoustic and articulatory populations. Such a distributed fronto-temporal circuit, in perisylvian cortex, is shown in Fig. 5a. The strict simultaneity of acoustic, phonological and lexical processing indexes is explained by this model, as neuronal populations in the same local structure, in superior-temporal cortex, are assumed to contribute to acoustic, phonological and lexical processes. Therefore, conduction times of the auditory input to these critical sites are roughly the same.3 The superior-temporal lobe indeed seems to contribute to all of these processes (Scott, 2005; Uppenkamp, Johnsrude, Norris, Marslen-Wilson, & Patterson, 2006) and the local activation differences between noise, phonemes and speech revealed by fMRI may be explained, in part, by differential linkage to articulatory circuits. Importantly, the evidence for stronger cortical activation (Pulvermüller et al., 2001) and motor links (Fadiga, Craighero, Buccino, & Rizzolatti, 2002; Watkins, Strafella, & Paus, 2003) of words compared with pseudowords supports the existence of action-perception circuits for spoken words. Further evidence that these lexical memory networks link superior-temporal (acoustic) circuits to inferior-frontal (speech motor planning) circuits comes from imaging work revealing coactivation of these areas in speech processing (Pulvermüller et al., 2003, 2006). The frontal areas involved are sparked 10–30 ms after superior-temporal activation (Pulvermüller et al., 2003), which is, as mentioned, consistent with direct measurements of conduction inter-area delays in cortex (Matsumoto et al., 2004). Note that a classic psycholinguistic model of a mixed parallel-and-cascaded nature could possibly be tailored to capture the experimental facts summarized; it would, however, not provide a priori predictions on the cortical areas involved and, critically, the time delay between area activations and psycholinguistic sub-processes.


Understanding in an instant: neurophysiological evidence for mechanistic language circuits in the brain.

Pulvermüller F, Shtyrov Y, Hauk O - Brain Lang (2009)

Lexical and semantic representations modelled at the mechanistic level of cortical circuits. As word learning implies linking spoken word forms to their respective articulatory patterns, the abstract articulatory acoustic pattern of a spoken word form is stored by strongly connected lexical circuits distributed over superior-temporal and inferior-frontal cortex (perisylvian cell assembly, a) In literate speakers, information about writing gestures and written word forms are bound to spoken word form representations; this binding of knowledge is cortically grounded in a halo of perisylvian cell assemblies extending into hand-related motor and premotor areas and fusiform gyrus (b). Meaningful words bind, in an arbitrary manner, information about their form and the concepts they refer to. Abstract semantic links are realized by the multiple connections between perisylvian cell assemblies and modality-specific semantic circuits in various parts of the cortex, for example in anterior- and inferior-temporal cortex (animal and color concepts, c), posterior-inferior and middle temporal cortex (tools and shapes, d), inferior-frontal cortex (face and articulatory actions, e), dorso-lateral fronto-central cortex (arm actions, f), and dorsal central cortex (leg actions, g). Ignition of these networks upon stimulation accounts for early near-simultaneity of neurocognitive indexes of psycholinguistic information access and conduction delays through long-distance cortico-cortical connections within these circuits explain fine-grained activation delays.
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC2734884&req=5

fig5: Lexical and semantic representations modelled at the mechanistic level of cortical circuits. As word learning implies linking spoken word forms to their respective articulatory patterns, the abstract articulatory acoustic pattern of a spoken word form is stored by strongly connected lexical circuits distributed over superior-temporal and inferior-frontal cortex (perisylvian cell assembly, a) In literate speakers, information about writing gestures and written word forms are bound to spoken word form representations; this binding of knowledge is cortically grounded in a halo of perisylvian cell assemblies extending into hand-related motor and premotor areas and fusiform gyrus (b). Meaningful words bind, in an arbitrary manner, information about their form and the concepts they refer to. Abstract semantic links are realized by the multiple connections between perisylvian cell assemblies and modality-specific semantic circuits in various parts of the cortex, for example in anterior- and inferior-temporal cortex (animal and color concepts, c), posterior-inferior and middle temporal cortex (tools and shapes, d), inferior-frontal cortex (face and articulatory actions, e), dorso-lateral fronto-central cortex (arm actions, f), and dorsal central cortex (leg actions, g). Ignition of these networks upon stimulation accounts for early near-simultaneity of neurocognitive indexes of psycholinguistic information access and conduction delays through long-distance cortico-cortical connections within these circuits explain fine-grained activation delays.
Mentions: Neuronal circuits processing spoken word forms comprise neurons in superior-temporal cortex activated by phonetic features of a spoken word, neurons in inferior-frontal cortex programming and controlling articulatory movements and additional neurons connecting the acoustic and articulatory populations. Such a distributed fronto-temporal circuit, in perisylvian cortex, is shown in Fig. 5a. The strict simultaneity of acoustic, phonological and lexical processing indexes is explained by this model, as neuronal populations in the same local structure, in superior-temporal cortex, are assumed to contribute to acoustic, phonological and lexical processes. Therefore, conduction times of the auditory input to these critical sites are roughly the same.3 The superior-temporal lobe indeed seems to contribute to all of these processes (Scott, 2005; Uppenkamp, Johnsrude, Norris, Marslen-Wilson, & Patterson, 2006) and the local activation differences between noise, phonemes and speech revealed by fMRI may be explained, in part, by differential linkage to articulatory circuits. Importantly, the evidence for stronger cortical activation (Pulvermüller et al., 2001) and motor links (Fadiga, Craighero, Buccino, & Rizzolatti, 2002; Watkins, Strafella, & Paus, 2003) of words compared with pseudowords supports the existence of action-perception circuits for spoken words. Further evidence that these lexical memory networks link superior-temporal (acoustic) circuits to inferior-frontal (speech motor planning) circuits comes from imaging work revealing coactivation of these areas in speech processing (Pulvermüller et al., 2003, 2006). The frontal areas involved are sparked 10–30 ms after superior-temporal activation (Pulvermüller et al., 2003), which is, as mentioned, consistent with direct measurements of conduction inter-area delays in cortex (Matsumoto et al., 2004). Note that a classic psycholinguistic model of a mixed parallel-and-cascaded nature could possibly be tailored to capture the experimental facts summarized; it would, however, not provide a priori predictions on the cortical areas involved and, critically, the time delay between area activations and psycholinguistic sub-processes.

Bottom Line: A key concept is that of discrete distributed cortical circuits with specific inter-area topographies.The full activation, or ignition, of specifically distributed binding circuits explains the near-simultaneity of early neurophysiological indexes of lexical, syntactic and semantic processing.Activity spreading within circuits determined by between-area conduction delays accounts for comprehension-related regional activation differences in the millisecond range.

View Article: PubMed Central - PubMed

Affiliation: Medical Research Council, Cognition and Brain Sciences Unit, 15 Chaucer Road, Cambridge, UK. friedemann.pulvermuller@mrc-cbu.cam.ac.uk

ABSTRACT
How long does it take the human mind to grasp the idea when hearing or reading a sentence? Neurophysiological methods looking directly at the time course of brain activity indexes of comprehension are critical for finding the answer to this question. As the dominant cognitive approaches, models of serial/cascaded and parallel processing, make conflicting predictions on the time course of psycholinguistic information access, they can be tested using neurophysiological brain activation recorded in MEG and EEG experiments. Seriality and cascading of lexical, semantic and syntactic processes receives support from late (latency approximately 1/2s) sequential neurophysiological responses, especially N400 and P600. However, parallelism is substantiated by early near-simultaneous brain indexes of a range of psycholinguistic processes, up to the level of semantic access and context integration, emerging already 100-250ms after critical stimulus information is present. Crucially, however, there are reliable latency differences of 20-50ms between early cortical area activations reflecting lexical, semantic and syntactic processes, which are left unexplained by current serial and parallel brain models of language. We here offer a mechanistic model grounded in cortical nerve cell circuits that builds upon neuroanatomical and neurophysiological knowledge and explains both near-simultaneous activations and fine-grained delays. A key concept is that of discrete distributed cortical circuits with specific inter-area topographies. The full activation, or ignition, of specifically distributed binding circuits explains the near-simultaneity of early neurophysiological indexes of lexical, syntactic and semantic processing. Activity spreading within circuits determined by between-area conduction delays accounts for comprehension-related regional activation differences in the millisecond range.

Show MeSH
Related in: MedlinePlus