A brain perspective on language mechanisms: from discrete neuronal ensembles to serial order

doi:10.1016/S0301-0082(02)00014-X

Progress in Neurobiology

Volume 67, Issue 2, June 2002, Pages 85-111

https://doi.org/10.1016/S0301-0082(02)00014-X Get rights and content

Abstract

Language is constituted by discrete building blocks, sounds and words, which can be concatenated according to serial order principles. The neurobiological organization of these building blocks, in particular words, has been illuminated by recent metabolic and neurophysiological imaging studies. When humans process words of different kinds, various sets of cortical areas have been found to become active differentially. The old concept of two language centers processing all words alike must therefore be replaced by a model according to which words are organized as discrete distributed neuron ensembles that differ in their cortical topographies. The meaning of a word, more precisely, aspects of its reference, may be crucial for determining which set of cortical areas becomes involved in its processing. Whereas the serial order of sounds constituting a word may be established by serially aligned sets of neurons called synfire chains, different mechanisms are necessary for establishing word order in sentences. The serial order of words may be organized by higher-order neuronal sets, called sequence detectors here, which are being activated by sequential excitation of neuronal sets representing words. Sets of sequence detectors are proposed to process aspects of the syntactic information contained in a sentence. Other syntactic rules can be related to general features of the dynamics of cortical activation and deactivation. These postulates about the brain mechanisms of language, which are rooted in principles known from neuroanatomy and neurophysiology, may provide a framework for theory-driven neuroscientific research on language.

Section snippets

Explaining language in terms of neurons

Recent advances in the neuroscientific investigation of cognition make it possible to spell out cognitive mechanisms in terms of neurons and to propose neuroscientific explanations of cognitive processes. An explanation deduces a variety of facts from a few principles or axioms. The axioms themselves must be non-disputable or well established by empirical evidence. This article shows that a few neuroscientific principles can explain important aspects of the neurophysiology of language. Four

Principles

The human cerebral cortex is a network of more than 10 billion neurons. Each neuron represents an information processor whose output is a function of the input it receives from many other neurons with which it is interwoven. The following principles are proposed to reflect universal neuroanatomical and neurophysiological properties of the human cortex:

(I)
Afferent and efferent projections are ordered. They reach, or take their origin from, well-defined areas within which the projections are

Functional webs in the cortex

The cortex is a network of neurons characterized by ordered input and output connections in modality-specific areas, by multimodal merging of information through short- and long-distance connections, and by correlation learning. Such a device can serve the function of linking neurons responding to specific features of input patterns and neurons controlling aspects of the motor output. Because different primary areas are not linked directly, additional neurons in non-primary areas are necessary

Functional cortical webs and their putative role in processing words

The cortex, a neuroanatomically defined associative memory obeying the correlation learning principle, allows for the formation of distributed functional webs. During language acquisition, the neurobiological principles governing the cortex give rise to the neuronal machinery underlying language. Three qualitatively different types of functional webs are proposed to be relevant for realizing spoken language in the cortex: networks linking information about articulatory movements and acoustic

Serial order in the brain

In language use, words usually occur in sequences. They are part of sentences of several words; although early in infancy, single-word utterances play an important role, and also later in life, communication using single-word utterances is common. The majority of utterances, however, are composed of several words that follow each other according to rules. How may the rules governing serial order of language elements be realized in the brain?

This question can be asked with regard to the level of

An overview of putative language mechanisms

The main proposals about language processing in the brain discussed in this review were the following:

(1)
Phonological word forms are represented and processed by strongly connected discrete neuron ensembles distributed over the perisylvian cortical areas and strongly lateralized to the language-dominant hemisphere. The activation of word-related functional webs may underlie the neurophysiological and metabolic differences between words and pseudo-words, in particular the early word-related

Acknowledgements

I thank Valentino Braitenberg, Almut Schüz, Bettina Mohr, and Ramin Assadollahi who, in countless discussions, contributed ideas to the framework presented here. The comments and stimulating input from the following colleagues are also thankfully acknowledged: Horace Barlow, Olaf Hauk, Sarah Hawkins, Detlef Heck, Markus Kiefer, William Marslen-Wilson, Peter M. Milner, Risto Näätänen, Bettina Neininger, Dennis Norris, Mike P. Page and Yury Shtyrov. I am grateful to Christine Zwierzanski for

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A brain perspective on language mechanisms: from discrete neuronal ensembles to serial order

Abstract

Section snippets

Explaining language in terms of neurons

Principles

Functional webs in the cortex

Functional cortical webs and their putative role in processing words

Serial order in the brain

An overview of putative language mechanisms

Acknowledgements

Brain Res.

Clin. Neurophysiol.

Brain Lang.

Cogn. Psychol.

Cognition

Brain Lang.

Neuron

Cognition

Neuropsychologia

Brain Res.

Neuropsychologia

Cogn. Sci.

Cogn. Brain Res.

Trends Neurosci.

Neuroimage

Brain Lang.

Neuroimage

Brain Lang.

Artif. Intell.

Trends Cogn. Sci.

Biophys. J.

Brain Lang.

Brain Lang.

Electroencephalogr. Clin. Neurophysiol.

Neuroimage

Neurosci. Lett.

Cognition

Spatiotemporal firing patterns in the frontal cortex of behaving monkeys

J. Neurophysiol.

Dependence of cortical plasticity on correlated activity of single neurons and on behavior context

Science

Neuromagnetic evidence for early access to cognitive representations

Neuroreport

Selective impairment of verb processing associated with pathological changes in Brodmann areas 44 and 45 in the motor neurone disease–dementia–aphasia syndrome

Brain

Single units and cognition: a neurone doctrine for perceptual psychology

Perception

The mechanism of directionally selective units in rabbit’s retina

J. Physiol.

Retinal ganglion cells responding selectively to direction and speed of image motion in the rabbit

J. Physiol.

From conceptual roles to structural relations: bridging the syntactic cleft

Psychol. Rev.

Entwurf einer neurologischen Theorie der Sprache

Naturwissenschaften

The detection and generation of sequences as a key to cerebellar function: experiments and theory

Behav. Brain Sci.

Remarques sur la siège de la faculté de la parole articulée, suivies d’une observation d’aphémie (perte de parole)

Bulletin de la Société d’Anatomie

Verb and noun meaning of homophone words activate different cortical generators: a topographic study of evoked potential fields

Exp. Brain Res.

Decoding temporal information: a model based on short-term synaptic plasticity

J. Neurosci.

Cortical plasticity: from synapses to maps

Annu. Rev. Neurosci.

Object and action naming in Alzheimer’s disease and frontotemporal dementia

Neurology

Development of language-specific phoneme representations in the infant brain

Nat. Neurosci.