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

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.     

Cerebral asymmetry: motoring on

I argue that the phylogenetic and neurobiological bases for cerebral asymmetry in humans are likely to be found in motor systems rather than in perceptual systems. Current genetic models of human laterality suggest that a `dextral' allele might be responsible for right-handedness and left-cerebral dominance for speech in the majority of humans. The linking of handedness with language lateralization might reflect the early evolution of language as predominantly a system of manual gestures, perhaps switching to a mainly vocal system only with the emergence of Homo sapiens. So-called `mirror neurons' in the prefrontal cortex of the monkey, which fire both when the animal makes a grasping response and when it sees the same response performed by others, might be part of a circuit that is the precursor to language circuits in the brain. This circuit appears to be bilateral in monkeys, but left-hemispheric in humans.     

Compositionality in a Parallel Architecture for Language Processing

Compositionality has been a central concept in linguistics and philosophy for decades, and it is increasingly prominent in many other areas of cognitive science. Its status, however, remains contentious. Here, I reassess the nature and scope of the principle of compositionality (Partee, 1995) from the perspective of psycholinguistics and cognitive neuroscience. First, I review classic arguments for compositionality and conclude that they fail to establish compositionality as a property of human language. Next, I state a new competence argument, acknowledging the fact that any competent user of a language L can assign to most expressions in L at least one meaning which is a function only of the meanings of the expression's parts and of its syntactic structure. I then discuss selected results from cognitive neuroscience, indicating that the human brain possesses the processing capacities presupposed by the competence argument. Finally, I outline a language processing architecture consistent with the neuroscience results, where semantic representations may be generated by a syntax-driven stream and by an “asyntactic” processing stream, jointly or independently. Compositionality is viewed as a constraint on computation in the former stream only.     

The roles of sequencing and verbal working memory in sentence comprehension deficits in Parkinson's disease

Studies of sentence comprehension deficits in Parkinson's disease (PD) patients suggest that language processing involves circuits connecting subcortical and cortical regions. Anatomically segregated neural circuits appear to support different cognitive and motor functions. To investigate which functions are implicated in PD comprehension deficits, we tested comprehension, verbal working memory span, and cognitive set-switching in a non-linguistic task in 41 PD patients; we also obtained speech measurements reflecting motor sequencing processes that may be involved in articulatory rehearsal within working memory. Comprehension of sentences with center-embedded or final relative clauses was impaired when they could not be understood from lexical semantic content alone. Overall comprehension error rates correlated strongly with impaired set-switching and significantly with reduced working memory span and speech motor sequencing deficits. Correlations with comprehension of different sentence structures indicate that these impairments do not represent a single deficit; rather, PD comprehension deficits appear to arise from several independent mechanisms. Deficits in cognitive set-switching or underlying inhibitory processes may compromise the ability to process relative clauses. Deficits in verbal working memory appear to impair comprehension of long-distance dependencies. Speech sequencing correlated with neither set-switching nor verbal working memory span, consistent with their being supported by independent, segregated cortico-subcortical circuits.     

Cognitive rehabilitation: attention and neglect

Cognitive neuroscience can make a significant contribution towards the development of a scientific basis for the practice of brain rehabilitation. Though rehabilitation is a vast worldwide industry, there is little scientific basis for the training and therapy that are designed to help damaged brain circuits to recover. The systematic application of cognitive neuroscience models to rehabilitation can not only foster better, more theoretically grounded rehabilitation, but the models themselves can be tested and modified by data generated in rehabilitation-oriented research. The example of unilateral spatial neglect is used here to show how non-intuitive but clinically tractable methods can emerge out of systematic application of cognitive neuroscience to the problem of how to foster dynamic change and recovery in the damaged brain. Examples are given of recently developed rehabilitation methods for unilateral spatial neglect that are both derived from theoretical models of cognitive function, and that feed back into these models. These include dorsal–ventral stream interactions, perceptuo–motor interactions, interhemispheric inhibitory dynamics, and arousal–spatial attention interactions. It will be to the mutual benefit of basic cognitive neuroscience and rehabilitation if this type of research is expanded into other domains of cognitive function, in which similar theory–practice interactions exist.     

Evolution of language: Lessons from the genome

The post-genomic era is an exciting time for researchers interested in the biology of speech and language. Substantive advances in molecular methodologies have opened up entire vistas of investigation that were not previously possible, or in some cases even imagined. Speculations concerning the origins of human cognitive traits are being transformed into empirically addressable questions, generating specific hypotheses that can be explicitly tested using data collected from both the natural world and experimental settings. In this article, I discuss a number of promising lines of research in this area. For example, the field has begun to identify genes implicated in speech and language skills, including not just disorders but also the normal range of abilities. Such genes provide powerful entry points for gaining insights into neural bases and evolutionary origins, using sophisticated experimental tools from molecular neuroscience and developmental neurobiology. At the same time, sequencing of ancient hominin genomes is giving us an unprecedented view of the molecular genetic changes that have occurred during the evolution of our species. Synthesis of data from these complementary sources offers an opportunity to robustly evaluate alternative accounts of language evolution. Of course, this endeavour remains challenging on many fronts, as I also highlight in the article. Nonetheless, such an integrated approach holds great potential for untangling the complexities of the capacities that make us human.     

Architecture and organizational principles of Broca's region

Identifying cortical areas for language and speech processing is a prerequisite for cognitive neuroscience and clinical research. Although Broca's region is one of the essential nodes in the language network, its anatomical constituents are ill-defined and multiple definitions of Broca's region exist. Sanides' concept of microstructural gradations interpreted Broca's region as developing from neighboring motor, dorsolateral-prefrontal, and insular cortices. Recent mapping approaches based on cytoarchitecture, transmitter receptor distribution, and connectivity revealed a highly differentiated segregation of this region far beyond Brodmann's classical scheme. This novel segregational concept of structural and functional architecture more adequately reflects the various functions of Broca's region in cognitive and/or linguistic processes.     

Neural evidence for the interplay between language, gesture, and action: a review

Co-speech gestures embody a form of manual action that is tightly coupled to the language system. As such, the co-occurrence of speech and co-speech gestures is an excellent example of the interplay between language and action. There are, however, other ways in which language and action can be thought of as closely related. In this paper we will give an overview of studies in cognitive neuroscience that examine the neural underpinnings of links between language and action. Topics include neurocognitive studies of motor representations of speech sounds, action-related language, sign language and co-speech gestures. It will be concluded that there is strong evidence on the interaction between speech and gestures in the brain. This interaction however shares general properties with other domains in which there is interplay between language and action.     

Neuroanatomical correlates of handedness for tool use in chimpanzees (Pan troglodytes): implication for theories on the evolution of language

It has been hypothesized that cognitive mechanisms underlying lateralized complex motor actions associated with tool use in chimpanzees may have set the stage for the evolution of left-hemisphere specialization for language and speech in humans. Here we report evidence that asymmetries in the homologues to Broca's and Wernicke's areas are associated with handedness for tool use in chimpanzees. These results suggest that the neural substrates of tool use may have served as a preadaptation for the evolution of language and speech in modern humans.     

Atypical speech lateralization in adults with developmental coordination disorder demonstrated using functional transcranial Doppler ultrasound

Research using clinical populations to explore the relationship between hemispheric speech lateralization and handedness has focused on individuals with speech and language disorders, such as dyslexia or specific language impairment (SLI). Such work reveals atypical patterns of cerebral lateralization and handedness in these groups compared to controls. There are few studies that examine this relationship in people with motor coordination impairments but without speech or reading deficits, which is a surprising omission given the prevalence of theories suggesting a common neural network underlying both functions. We use an emerging imaging technique in cognitive neuroscience; functional transcranial Doppler (fTCD) ultrasound, to assess whether individuals with developmental coordination disorder (DCD) display reduced left‐hemisphere lateralization for speech production compared to control participants. Twelve adult control participants and 12 adults with DCD, but no other developmental/cognitive impairments, performed a word‐generation task whilst undergoing fTCD imaging to establish a hemispheric lateralization index for speech production. All participants also completed an electronic peg‐moving task to determine hand skill. As predicted, the DCD group showed a significantly reduced left lateralization pattern for the speech production task compared to controls. Performance on the motor skill task showed a clear preference for the dominant hand across both groups; however, the DCD group mean movement times were significantly higher for the non‐dominant hand. This is the first study of its kind to assess hand skill and speech lateralization in DCD. The results reveal a reduced leftwards asymmetry for speech and a slower motor performance. This fits alongside previous work showing atypical cerebral lateralization in DCD for other cognitive processes (e.g., executive function and short‐term memory) and thus speaks to debates on theories of the links between motor control and language production.     

Mirror neurons and embodied simulation in the development of archetypes and self-agency

Abstract :  In this paper I explore the role of mirror neurons and motor intentionality in the development of self-agency. I suggest that this will also give us a firmer basis for an emergent view of archetypes, as key components in the development trajectory of self-agency, from its foundation in bodily action to its mature expression in mentalization and a conscious awareness of intentionality. I offer some ideas about the implications of these issues of self-agency for our clinical work with patients whose developmental trajectory of self-agency has been partially inhibited, so that their communications have a coercive effect. I discuss the possibility that this kind of clinical phenomenon may relate to Gallese and Lakoff's hypothesis that abstract thought and imagination are forms of simulated action, and that the same sensory-motor circuits that control action also control imagination, concept formation and understanding, but with a crucial development, that of an inhibition of the connections between secondary pre-motor cortical areas and the primary motor cortex. I shall speculate that in the earlier developmental stages of self-agency, the separation of secondary from primary motor areas is not complete, so that imagination and thought are not entirely independent of physical action.     

Language as gesture

Language can be understood as an embodied system, expressible as gestures. Perception of these gestures depends on the “mirror system,” first discovered in monkeys, in which the same neural elements respond both when the animal makes a movement and when it perceives the same movement made by others. This system allows gestures to be understood in terms of how they are produced, as in the so-called motor theory of speech perception. I argue that human speech evolved from manual gestures, with vocal gestures being gradually incorporated into the mirror system in the course of hominin evolution. Speech may have become the dominant mode only with the emergence of Homo sapiens some 170,100 years ago, although language as a relatively complex syntactic system probably emerged over the past 2 million years, initially as a predominantly manual system. Despite the present-day dominance of speech, manual gestures accompany speech, and visuomanual forms of language persist in signed languages of the deaf, in handwriting, and even in such forms as texting.     

Pre-frontal executive committee for perception,working memory,attention, long-term memory,motor control,and thinking: a tutorial review

As an explicit organizing metaphor, memory aid, and conceptual framework, the prefrontal cortex may be viewed as a five-member 'Executive Committee,' as the prefrontal-control extensions of five sub-and-posterior-cortical systems: (1) the 'Perceiver' (dominant-right-hemisphere ventral-lateral prefrontal cortex--VL/PERC-PFC) is the frontal extension of the ventral perceptual stream (the VL/PERC system) which represents the world and self in object coordinates; (2) the 'Verbalizer' (dominant-left-hemisphere ventral-lateral prefrontal cortex system--VL/VERB-PFC) is the frontal extension of the language stream (the VL/VERB system) which represents the world and self in language coordinates; (3) the 'Motivator' (ventral/medial-orbital pre-frontal cortex--VMO-PFC) is the frontal cortical extension of a subcortical extended-amygdala stream (the VMO system) which represents the world and self in motivational/emotional coordinates; (4) the 'Attender' (dorsal-medial/anterior cingulate--DM/AC-PFC) is the frontal cortical extension of a subcortical extended-hippocampal stream (the DM/AC system) which represents the world and self in spatiotemporal coordinates and directs attention to internal and external events; and (5) the 'Coordinator' (the dorsolateral prefrontal cortex--DL-PFC) is the frontal extension of the dorsal perceptual stream (the DL system) which represents the world and self in body- and eye-coordinates and controls willed action and working memory. This tutorial review examines the interacting roles of these five systems in perception, working memory, attention, long-term memory, motor control, and thinking.     

Sensori‐motor experience leads to changes in visual processing in the developing brain

Since Broca’s studies on language processing, cortical functional specialization has been considered to be integral to efficient neural processing. A fundamental question in cognitive neuroscience concerns the type of learning that is required for functional specialization to develop. To address this issue with respect to the development of neural specialization for letters, we used functional magnetic resonance imaging (fMRI) to compare brain activation patterns in pre‐school children before and after different letter‐learning conditions: a sensori‐motor group practised printing letters during the learning phase, while the control group practised visual recognition. Results demonstrated an overall left‐hemisphere bias for processing letters in these pre‐literate participants, but, more interestingly, showed enhanced blood oxygen‐level‐dependent activation in the visual association cortex during letter perception only after sensori‐motor (printing) learning. It is concluded that sensori‐motor experience augments processing in the visual system of pre‐school children. The change of activation in these neural circuits provides important evidence that ‘learning‐by‐doing’ can lay the foundation for, and potentially strengthen, the neural systems used for visual letter recognition.     

The finger in flight: real-time motor control by visually masked color stimuli

Current theories of dual visual systems suggest that color is processed in a ventral cortical stream that eventually gives rise to visual awareness but is only indirectly involved in visuomotor control mediated by the dorsal stream. If the dorsal stream is indeed less sensitive to color than the ventral stream, color stimuli blocked from awareness by visual masking should also be blocked from guiding fast motor responses. In this study, pointing movements to one of two isoluminant color targets were preceded by consistent or inconsistent color primes. Trajectories were strongly affected by priming, with kinematics implying a continuous flow of color information into executive brain areas while the finger was already moving. Motor effects were more sensitive to color of the primes than were deliberate attempts to identify the primes in forced-choice tasks based on visual awareness. Priming was observed even when masking was complete.     

Selectionist Approaches in Evolutionary Linguistics: An Epistemological Analysis

Evolutionary linguistics is methodologically inspired by evolutionary psychology and the neo-Darwinian, selectionist approach. Language is claimed to have evolved by means of natural selection. The focus therefore lies not on how language evolved, but on finding out why language evolved. This latter question is answered by identifying the functional benefits and adaptive status that language provides, from which in turn selective pressures are deduced. This article analyses five of the most commonly given pressures or reasons why presumably language evolved. I demonstrate that these reasons depend on functional definitions of what language is. To undo this bias, I suggest that scholars move away from the ‘why’ and ‘what for’ questions of language evolution, and focus on how language actually evolved. The latter project inquires into the distinct evolutionary mechanisms enabling the evolution of the anatomical and sociocultural traits underlying linguistic behaviour.     

Language and motor abilities of preschool children who stutter: Evidence from behavioral and kinematic indices of nonword repetition performance

Stuttering is a disorder of speech production that typically arises in the preschool years, and many accounts of its onset and development implicate language and motor processes as critical underlying factors. There have, however, been very few studies of speech motor control processes in preschool children who stutter. Hearing novel nonwords and reproducing them engages multiple neural networks, including those involved in phonological analysis and storage and speech motor programming and execution. We used this task to explore speech motor and language abilities of 31 children aged 4–5 years who were diagnosed as stuttering. We also used sensitive and specific standardized tests of speech and language abilities to determine which of the children who stutter had concomitant language and/or phonological disorders. Approximately half of our sample of stuttering children had language and/or phonological disorders. As previous investigations would suggest, the stuttering children with concomitant language or speech sound disorders produced significantly more errors on the nonword repetition task compared to typically developing children. In contrast, the children who were diagnosed as stuttering, but who had normal speech sound and language abilities, performed the nonword repetition task with equal accuracy compared to their normally fluent peers. Analyses of interarticulator motions during accurate and fluent productions of the nonwords revealed that the children who stutter (without concomitant disorders) showed higher variability in oral motor coordination indices. These results provide new evidence that preschool children diagnosed as stuttering lag their typically developing peers in maturation of speech motor control processes.Educational objectives: The reader will be able to: (a) discuss why performance on nonword repetition tasks has been investigated in children who stutter; (b) discuss why children who stutter in the current study had a higher incidence of concomitant language deficits compared to several other studies; (c) describe how performance differed on a nonword repetition test between children who stutter who do and do not have concomitant speech or language deficits; (d) make a general statement about speech motor control for nonword production in children who stutter compared to controls.     

Toward the Language-Ready Brain: Biological Evolution and Primate Comparisons

The approach to language evolution suggested here focuses on three questions: How did the human brain evolve so that humans can develop, use, and acquire languages? How can the evolutionary quest be informed by studying brain, behavior, and social interaction in monkeys, apes, and humans? How can computational modeling advance these studies? I hypothesize that the brain is language ready in that the earliest humans had protolanguages but not languages (i.e., communication systems endowed with rich and open-ended lexicons and grammars supporting a compositional semantics), and that it took cultural evolution to yield societies (a cultural constructed niche) in which language-ready brains could become language-using brains. The mirror system hypothesis is a well-developed example of this approach, but I offer it here not as a closed theory but as an evolving framework for the development and analysis of conflicting subhypotheses in the hope of their eventual integration. I also stress that computational modeling helps us understand the evolving role of mirror neurons, not in and of themselves, but only in their interaction with systems “beyond the mirror.” Because a theory of evolution needs a clear characterization of what it is that evolved, I also outline ideas for research in neurolinguistics to complement studies of the evolution of the language-ready brain. A clear challenge is to go beyond models of speech comprehension to include sign language and models of production, and to link language to visuomotor interaction with the physical and social world.     

Context-sensitive binding by the laminar circuits of V1 and V2: A unified model of perceptual grouping,attention, and orientation contrast

A detailed neural model is presented of how the laminar circuits of visual cortical areas V1 and V2 implement context-sensitive binding processes such as perceptual grouping and attention. The model proposes how specific laminar circuits allow the responses of visual cortical neurons to be determined not only by the stimuli within their classical receptive fields, but also to be strongly influenced by stimuli in the extra-classical surround. This context-sensitive visual processing can greatly enhance the analysis of visual scenes, especially those containing targets that are low contrast, partially occluded, or crowded by distractors. We show how interactions of feedforward, feedback, and horizontal circuitry can implement several types of contextual processing simultaneously, using shared laminar circuits. In particular, we present computer simulations that suggest how top-down attention and preattentive perceptual grouping, two processes that are fundamental for visual binding, can interact, with attentional enhancement selectively propagating along groupings of both real and illusory contours, thereby showing how attention can selectively enhance object representations. These simulations also illustrate how attention may have a stronger facilitatory effect on low contrast than on high contrast stimuli, and how pop-out from orientation contrast may occur. The specific functional roles which the model proposes for the cortical layers allow several testable neurophysiological predictions to be made. The results presented here simulate only the boundary grouping system of adult cortical architecture. However, we also discuss how this model contributes to a larger neural theory of vision that suggests how intracortical and intercortical feedback help to stabilize development and learning within these cortical circuits. Although feedback plays a key role, fast feedforward processing is possible in response to unambiguous information. Model circuits are capable of synchronizing quickly, but context-sensitive persistence of previous events can influence how synchrony develops. Although these results focus on how the interblob cortical processing stream controls boundary grouping and attention, related modelling of the blob cortical processing stream suggests how visible surfaces are formed, and modelling of the motion stream suggests how transient responses to scenic changes can control long-range apparent motion and also attract spatial attention.     

Neurophysiologic markers of primary motor cortex for laryngeal muscles and premotor cortex in caudal opercular part of inferior frontal gyrus investigated in motor speech disorder: a navigated transcranial magnetic stimulation (TMS) study

Transcranial magnetic stimulation studies have so far reported the results of mapping the primary motor cortex (M1) for hand and tongue muscles in stuttering disorder. This study was designed to evaluate the feasibility of repetitive navigated transcranial magnetic stimulation (rTMS) for locating the M1 for laryngeal muscle and premotor cortical area in the caudal opercular part of inferior frontal gyrus, corresponding to Broca’s area in stuttering subjects by applying new methodology for mapping these motor speech areas. Sixteen stuttering and eleven control subjects underwent rTMS motor speech mapping using modified patterned rTMS. The subjects performed visual object naming task during rTMS applied to the (a) left M1 for laryngeal muscles for recording corticobulbar motor-evoked potentials (CoMEP) from cricothyroid muscle and (b) left premotor cortical area in the caudal opercular part of inferior frontal gyrus while recording long latency responses (LLR) from cricothyroid muscle. The latency of CoMEP in control subjects was 11.75 ± 2.07 ms and CoMEP amplitude was 294.47 ± 208.87 µV, and in stuttering subjects CoMEP latency was 12.13 ± 0.75 ms and 504.64 ± 487.93 µV CoMEP amplitude. The latency of LLR in control subjects was 52.8 ± 8.6 ms and 54.95 ± 4.86 in stuttering subjects. No significant differences were found in CoMEP latency, CoMEP amplitude, and LLR latency between stuttering and control-fluent speakers. These results indicate there are probably no differences in stuttering compared to controls in functional anatomy of the pathway used for transmission of information from premotor cortex to the M1 cortices for laryngeal muscle representation and from there via corticobulbar tract to laryngeal muscles.