Dorsal and ventral streams: a framework for understanding aspects of the functional anatomy of language

doi:10.1016/j.cognition.2003.10.011

Cognition

Volume 92, Issues 1–2, May–June 2004, Pages 67-99

https://doi.org/10.1016/j.cognition.2003.10.011 Get rights and content

Abstract

Despite intensive work on language–brain relations, and a fairly impressive accumulation of knowledge over the last several decades, there has been little progress in developing large-scale models of the functional anatomy of language that integrate neuropsychological, neuroimaging, and psycholinguistic data. Drawing on relatively recent developments in the cortical organization of vision, and on data from a variety of sources, we propose a new framework for understanding aspects of the functional anatomy of language which moves towards remedying this situation. The framework posits that early cortical stages of speech perception involve auditory fields in the superior temporal gyrus bilaterally (although asymmetrically). This cortical processing system then diverges into two broad processing streams, a ventral stream, which is involved in mapping sound onto meaning, and a dorsal stream, which is involved in mapping sound onto articulatory-based representations. The ventral stream projects ventro-laterally toward inferior posterior temporal cortex (posterior middle temporal gyrus) which serves as an interface between sound-based representations of speech in the superior temporal gyrus (again bilaterally) and widely distributed conceptual representations. The dorsal stream projects dorso-posteriorly involving a region in the posterior Sylvian fissure at the parietal–temporal boundary (area Spt), and ultimately projecting to frontal regions. This network provides a mechanism for the development and maintenance of “parity” between auditory and motor representations of speech. Although the proposed dorsal stream represents a very tight connection between processes involved in speech perception and speech production, it does not appear to be a critical component of the speech perception process under normal (ecologically natural) listening conditions, that is, when speech input is mapped onto a conceptual representation. We also propose some degree of bi-directionality in both the dorsal and ventral pathways. We discuss some recent empirical tests of this framework that utilize a range of methods. We also show how damage to different components of this framework can account for the major symptom clusters of the fluent aphasias, and discuss some recent evidence concerning how sentence-level processing might be integrated into the framework.

Section snippets

Introduction and preliminaries

The functional anatomic framework for language which is presented in this paper is based on a rather old insight in language research dating back at least to the 19th century (e.g. Wernicke, 1874/1969), namely that sensory speech codes must minimally interface with two systems: a conceptual system and a motor–articulatory system. The existence of an interface with the conceptual system requires no motivation; such an interface is required if we are to comprehend the meaning of the words we

Overview of the framework

The framework we have proposed (Hickok & Poeppel, 2000) and further develop here draws heavily on what is known about the functional anatomy of vision, and more recently audition, particularly the distinction that has been made between dorsal and ventral streams. Most of the discussion of dorsal and ventral streams in the literature centers on the concept of “where” and “what” pathways (Ungerleider & Mishkin, 1982). The fundamental distinction proposed by Ungerleider and Mishkin was that visual

Task dissociations in “speech perception”

One central thesis of our approach is that the execution of different linguistic tasks (functions) involves non-identical neural networks, even with stimulus conditions held constant. In this section we review evidence that supports this assumption in the domain of speech perception. In particular, the evidence shows that the ability to perform sub-lexical speech tasks (phoneme identification, rhyming tasks, and so on) double-dissociates from the ability to comprehend words (which presumably

The ventral stream

The ventral stream, which one can broadly conceptualize as an auditory ‘what’ system, deals with the conversion of sensory information into a format suitable for linguistic computation (in the case of speech input). As such, this pathway deals with (probably multiple levels of) acoustic–phonetic processing, the interface of acoustic–phonetic representations with lexical representations, and the interface of the lexical items or roots with the computational system responsible for syntactic and

The dorsal stream

Using the organization of the visual system as a guide, we have hypothesized the existence of a dorsal auditory stream which is critical for auditory–motor integration (Hickok & Poeppel, 2000). In this section we first outline current views on dorsal-stream sensory–motor integration networks in vision, and then specify the role that an auditory–motor integration system might play in speech/language. Finally, we turn to neural evidence relevant to mapping the spatial distribution of this network.

Perception–production overlap in posterior “sensory” cortex

A critical component of Wernicke's 1874 model was that auditory representations of speech played an important role in speech production; this is how speech production errors (paraphasias) were explained in aphasia caused by lesions to left auditory areas. Available evidence suggests he was correct (Buchsbaum et al., 2001, Hickok, 2001, Hickok et al., 2000).

Some of the best evidence comes from conduction aphasia (Hickok, 2000). Such patients have two primary deficits, phonemic paraphasias in

Understanding aphasia

The framework outlined in this article and schematized in Fig. 1 is in part motivated by findings from the deficit-lesion literature and should account in natural ways for relevant aphasic syndromes. Here we summarize how the proposal provides a framework to discuss deficit-lesion data using four types of clinical deficits.

Summary and conclusions

The framework for the functional anatomy of language which we have outlined here has strengths and weaknesses. The limitations are straightforward. It is very broad in scope, and therefore glosses over many important details: what exactly is an “acoustic–phonetic representation of speech”? What are the computations involved in mapping sound onto meaning, or auditory onto motor representations? (However, some existing models may fit well into the current framework, as suggested above.) It does

Acknowledgements

This work has benefited from many discussions and correspondences with colleagues and students including Kathy Baines, Laura Barde, Brad Buchsbaum, Hugh Buckingham, Nina Dronkers, Nicole Gage, Jack Gandour, Colin Humphries, John Jonides, Sophie Scott, and Richard Wise. We are also grateful to four Cognition reviewers who provided excellent and constructive comments on this manuscript. This work was supported by NIH grant R01DC0361 (G.H.), and by NIH R01DC 05660 (D.P.). During the preparation of

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Dorsal and ventral streams: a framework for understanding aspects of the functional anatomy of language

Abstract

Section snippets

Introduction and preliminaries

Overview of the framework

Task dissociations in “speech perception”

The ventral stream

The dorsal stream

Perception–production overlap in posterior “sensory” cortex

Understanding aphasia

Summary and conclusions

Acknowledgements

Brain Research Reviews

Current Biology

Brain and Language

Neuropsychologia

Brain and Language

Neuropsychologia

Neuropsychologia

Cognitive Science

Trends in Cognitive Sciences

Journal of Neurolinguistics

Brain and Language

Brain Research

Neuroscience Letters

Trends in Cognitive Sciences

Cognition

Cognition

Cognitive Psychology

Brain and Language

Brain and Language

Cognition

Neuroscience Letters

Cognitive Science

Speech Communication

Current Opinion in Neurobiology

Current Opinion in Neurobiology

Brain and Language

Journal of Verbal Learning and Verbal Behavior

Speech production and comprehension: one lexicon or two?

Multimodal integration for the representation of space in the posterior parietal cortex

Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences

Dissociation of storage and rehearsal in working memory: PET evidence

Psychological Science

Working memory

Science

“Phonemic” perception in aphasia and in the isolated right hemisphere

Cognitive Neuroscience Society Annual Meeting Program

Phonemic identification defects in aphasia

Cortex

“What”, “where” and “how” in auditory cortex

Nature Neuroscience

Lateralization of speech and auditory temporal processing

Journal of Cognitive Neuroscience

Conduction aphasia: a clinicopathological study

Archives of Neurology

Human temporal lobe activation by speech and nonspeech sounds

Cerebral Cortex

Human brain language areas identified by functional magnetic resonance imaging

Journal of Neuroscience

Word deafness: one hundred years later

Journal of Neurology, Neurosurgery, and Psychiatry

A new perspective on the functional anatomy of phonological working memory: fMRI investigations

Cognitive Neuroscience Society Eighth Annual Meeting Program

The role of segmentation in phonological processing: an fMRI investigation

Journal of Cognitive Neuroscience

Analysis of lesions by MRI in stroke patients with acoustic-phonetic processing deficits

Neurology

Location of lesions in stroke patients with deficits in syntactic processing in sentence comprehension

Brain

How many levels of processing are there in lexical access?

Cognitive Neuropsychology

The brain binds entities and events by multiregional activation from convergence zones

Neural Computation

Aphasia

New England Journal of Medicine

Neuroanatomical correlates of the aphasias

The anatomical basis of conduction aphasia

Brain