The Developmental Trajectory from Amodal Perception to Empathy and Communication: The Role of Mirror Neurons in This Process

In a recent paper entitled “Mirror Neurons. Procedural Learning and the Positive New Experience” (Wolf et al., 2000), data were presented about a special type of neuron, the mirror neuron, originally located by Rizzolatti and his colleagues (1995). These neurons were discussed as they related to a particular developmental view of psychoanalysis, developmental systems self psychology (Shane, Shane, and Gales. 1997).

In this paper, we focus on how this mirror neuron system might contribute to the development of communicative abilities in humans. First we summarize the research findings about mirror neurons and how they apply to humans. We then attempt to demonstrate how the mirror neuron system might be involved in a developmental sequence hypothesized by Kohut (1984), Stern (1985), and others to begin in infancy. We postulate that this trajectory starts with the onset of “amodal perception” (Stern, 1985) and then proceeds to affect resonance, joint attention, and ultimately to symbolization of language. In this paper, we attempt to integrate these concepts with a formulation of empathy and demonstrate what might go awry in developmental disorders when the normative sequence of development described above does not take place.     

NONVOCAL LANGUAGE ACQUISITION IN ADOLESCENTS WITH SEVERE PHYSICAL DISABILITIES: BLISSYMBOL VERSUS ICONIC STIMULUS FORMATS

This study compared training in two language systems for three severely handicapped, nonvocal adolescents: the Bliss symbol system and an iconic picture system. Following baseline, training and review trials were implemented using an alternating treatments design. Daily probes were conducted to assess maintenance, stimulus generalization, and response generalization, and data were collected on spontaneous usage of either language system throughout the school day. Results showed that students required approximately four times as many trials to acquire Bliss symbols as iconic pictures, and that students maintained a higher percentage of iconic pictures. Stimulus generalization occurred in both language systems, while the number of correct responses during responses generalization probes was much greater for the iconic system. Finally, students almost always showed more iconic responses than Bliss responses in daily spontaneous usage. These results suggest that an iconic system might be more readily acquired, maintained, and generalized to daily situations. Implications of these findings for the newly verbal person were discussed.     

A cortical circuit for voluntary laryngeal control: Implications for the evolution language

The development of voluntary laryngeal control has been argued to be a key innovation in the evolution of language. Part of the evidence for this hypothesis comes from neuroscience. For example, comparative research has shown that humans have direct cortical innervation of motor neurons controlling the larynx, whereas nonhuman primates do not. Research on cortical motor control circuits has shown that the frontal lobe cortical motor system does not work alone; it is dependent on sensory feedback control circuits. Thus, the human brain must have evolved not only the required efferent motor pathway but also the cortical circuit for controlling those efferent signals. To fill this gap, I propose a link between the evolution of laryngeal control and neuroscience research on the human dorsal auditory-motor speech stream. Specifically, I argue that the dorsal stream Spt (Sylvian parietal-temporal) circuit evolved in step with the direct cortico-laryngeal control pathway and together represented a key advance in the evolution of speech. I suggest that a cortical laryngeal control circuit may play an important role in language by providing a prosodic frame for speech planning.     

The search for phonology in other species

Human language draws on a complex set of cognitive, motor and auditory skills. Some of these are found in other species but others are thought to be absent. There has been a burst of research in this area over the past five years, both in examining natural communication systems and also in the laboratory, exposing animals to human language. Most of the work has focused on analogies to syntax. Although many of the fundamental building blocks for basic phonological skills might be found outside humans, most aspects of core phonology have never been investigated.     

The emergence of a new paradigm in ape language research

In recent years we have seen a dramatic shift, in several different areas of communication studies, from an information-theoretic to a dynamic systems paradigm. In an information processing system, communication, whether between cells, mammals, apes, or humans, is said to occur when one organism encodes information into a signal that is transmitted to another organism that decodes the signal. In a dynamic system, all of the elements are continuously interacting with and changing in respect to one another, and an aggregate pattern emerges from this mutual co-action. Whereas the information-processing paradigm looks at communication as a linear, binary sequence of events, the dynamic systems paradigm looks at the relation between behaviors and how the whole configuration changes over time. One of the most dramatic examples of the significance of shifting from an information processing to a dynamic systems paradigm can be found in the debate over the interpretation of recent advances in ape language research (ALR). To some extent, many of the early ALR studies reinforced the stereotype that animal communication is functional and stimulus bound, precisely because they were based on an information-processing paradigm that promoted a static model of communicative development. But Savage-Rumbaugh's recent results with bonobos has introduced an entirely new dimension into this debate. Shifting the terms of the discussion from an information-processing to a dynamic systems paradigm not only highlights the striking differences between Savage-Rumbaugh's research and earlier ALR studies, but further, it sheds illuminating light on the factors that underpin the development of communication skills in great apes and humans, and the relationship between communicative development and the development of language.     

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.     

Cognitive and emotional influences in anterior cingulate cortex

Anterior cingulate cortex (ACC) is a part of the brain's limbic system. Classically, this region has been related to affect, on the basis of lesion studies in humans and in animals. In the late 1980s, neuroimaging research indicated that ACC was active in many studies of cognition. The findings from EEG studies of a focal area of negativity in scalp electrodes following an error response led to the idea that ACC might be the brain's error detection and correction device. In this article, these various findings are reviewed in relation to the idea that ACC is a part of a circuit involved in a form of attention that serves to regulate both cognitive and emotional processing. Neuroimaging studies showing that separate areas of ACC are involved in cognition and emotion are discussed and related to results showing that the error negativity is influenced by affect and motivation. In addition, the development of the emotional and cognitive roles of ACC are discussed, and how the success of this regulation in controlling responses might be correlated with cingulate size. Finally, some theories are considered about how the different subdivisions of ACC might interact with other cortical structures as a part of the circuits involved in the regulation of mental and emotional activity.     

Processing abstract language modulates motor system activity

Embodiment theory proposes that neural systems for perception and action are also engaged during language comprehension. Previous neuroimaging and neurophysiological studies have only been able to demonstrate modulation of action systems during comprehension of concrete language. We provide neurophysiological evidence for modulation of motor system activity during the comprehension of both concrete and abstract language. In Experiment 1, when the described direction of object transfer or information transfer (e.g., away from the reader to another) matched the literal direction of a hand movement used to make a response, speed of responding was faster than when the two directions mismatched (an action-sentence compatibility effect). In Experiment 2, we used single-pulse transcranial magnetic stimulation to study changes in the corticospinal motor pathways to hand muscles while reading the same sentences. Relative to sentences that do not describe transfer, there is greater modulation of activity in the hand muscles when reading sentences describing transfer of both concrete objects and abstract information. These findings are discussed in relation to the human mirror neuron system.     

Linguistically mediated visual search

During an individual's normal interaction with the environment and other humans, visual and linguistic signals often coincide and can be integrated very quickly. This has been clearly demonstrated in recent eyetracking studies showing that visual perception constrains on-line comprehension of spoken language. In a modified visual search task, we found the inverse, that real-time language comprehension can also constrain visual perception. In standard visual search tasks, the number of distractors in the display strongly affects search time for a target defined by a conjunction of features, but not for a target defined by a single feature. However, we found that when a conjunction target was identified by a spoken instruction presented concurrently with the visual display, the incremental processing of spoken language allowed the search process to proceed in a manner considerably less affected by the number of distractors. These results suggest that perceptual systems specialized for language and for vision interact more fluidly than previously thought.     

Language and space: some interactions

Is language linked to mental representations of space? There are several reasons to think that language and space might be separated in our cognitive systems, but they nevertheless interact in important ways. These interactions are evident in language viewed as a means of communication and in language considered a form of representation. In communication, spatial factors may be explicit in language itself, such as the spatial-gestural system of American Sign Language. Even the act of conversing with others is a spatial behavior because we orient to the locations of other participants. Language and spatial representations probably converge at an abstract level of concepts and simple spatial schemas.     

Evolution of the neural language network

The evolution of language correlates with distinct changes in the primate brain. The present article compares language-related brain regions and their white matter connectivity in the developing and mature human brain with the respective structures in the nonhuman primate brain. We will see that the functional specificity of the posterior portion of Broca’s area (Brodmann area [BA 44]) and its dorsal fiber connection to the temporal cortex, shown to support the processing of structural hierarchy in humans, makes a crucial neural difference between the species. This neural circuit may thus be fundamental for the human syntactic capacity as the core of language.     

A neuronal retuning hypothesis of sentence-specificity in Broca’s area

It is clear that the left inferior frontal gyrus (LIFG) contributes in some fashion to sentence processing. While neuroimaging and neuropsychological evidence support a domain-general working memory function, recent neuroimaging data show that particular subregions of the LIFG, particularly the pars triangularis (pTri), show selective activation for sentences relative to verbal working memory and cognitive control tasks. These data suggest a language-specific function rather than a domain-general one. To resolve this apparent conflict, I propose separating claims of domain-generality and specificity independently for computations and representations—a given brain region may respond to a specific representation while performing a general computation over that representation, one shared with other systems. I hypothesize that the pTri underlies a language-specific working memory system, comprised of general memory retrieval/attention operations specialized for syntactic representations. There is a parallelism of top-down retrieval function among the phonological and semantic levels, localized to the pars opercularis and pars orbitalis, respectively. I further explore the idea of how such a system emerges in the human brain through the framework of neuronal retuning: the “borrowing” of domain-general mechanisms for language, either in evolution or development. The empirical data appear to tentatively support a developmental account of language-specificity in the pTri, possibly through connections to the posterior superior temporal sulcus (pSTS), a region that is both anatomically distinct for humans and functionally essential for language. Evidence of representational response specificity obtained from neuroimaging studies is useful in understanding how cognition is implemented in the brain. However, understanding the shared computations across domains and neural systems is necessary for a fuller understanding of this problem, providing potential answers to questions of how specialized systems, such as language, are implemented in the brain.     

Death and the Evolution of Language

My hypothesis is that the cognitive challenge posed by death might have had a co-evolutionary role in the development of linguistic faculties. First, I claim that mirror neurons, which enable us to understand others’ actions and emotions, not only activate when we directly observe someone, but can also be triggered by language: words make us feel bodily sensations. Second, I argue that the death of another individual cannot be understood by virtue of the mirror neuron mechanism, since the dead provide no neural pattern for mirroring: this cognitive task requires symbolic thought, which in turn involves emotions. Third, I describe the symbolic leap of the human species as a cognitive detachment from the here and now, allowing displaced reference: through symbols the human mind can refer to what is absent, possible, or even impossible (like the presence of a dead person). Such a detachment has had a huge adaptive impact: adopting a coevolutionary standpoint can help explain why language is as effective as environmental inputs in order to stimulate our bodily experience. In the end I suggest a further coevolutionary “reversal”: if language is necessary to understand the death of the other, it might also be true that the peculiar cognitive problem posed by the death of the other (the corpse is present, but the other is absent) has contributed to the crucial transition from an indexical sign system to the symbolic level, i.e., the “cognitive detachment”. Death and language, as Heidegger claimed, have an essential relation for humans, both from an evolutionary and a phenomenological perspective: they have shaped the symbolic consciousness that make us conceive of them.     

Continuity of the conceptual system across species

In a recent neuroimaging study of macaque monkeys, Gil-da-Costa and colleagues reported that a distributed circuit of modality-specific properties represents macaques' conceptual knowledge of social situations. The circuit identified shows striking similarities to analogous circuits in humans that represent conceptual knowledge. This parallel suggests that a common architecture underlies the conceptual systems of different species, although with additional systems extending human conceptual abilities significantly.     

Rhesus monkeys (Macaca mulatta) immediately generalize the uncertain response

Rhesus monkeys (Macaca mulatta) have learned, like humans, to use an uncertain response adaptively under test conditions that create uncertainty, suggesting a metacognitive process by which human and nonhuman primates may monitor their confidence and alter their behavior accordingly. In this study, 4 rhesus monkeys generalized their use of the uncertain response, without additional training, to 2 familiar tasks (2-choice discrimination learning and mirror-image matching to sample) that predictably and demonstrably produce uncertainty. The monkeys were significantly less likely to use the uncertain response on trials in which the answer might be known. These results indicate that monkeys, like humans, know when they do not know and that they can learn to use a symbol as a generalized means for indicating their uncertainty.     

Computer-based assessment of student-constructed responses

Student-constructed responses, such as essays, short-answer questions, and think-aloud protocols, provide a valuable opportunity to gauge student learning outcomes and comprehension strategies. However, given the challenges of grading student-constructed responses, instructors may be hesitant to use them. There have been major advances in the application of natural language processing of student-constructed responses. This literature review focuses on two dimensions that need to be considered when developing new systems. The first is type of response provided by the student-namely, meaning-making responses (e.g., think-aloud protocols, tutorial dialogue) and products of comprehension (e.g., essays, open-ended questions). The second corresponds to considerations of the type of natural language processing systems used and how they are applied to analyze the student responses. We argue that the appropriateness of the assessment protocols is, in part, constrained by the type of response and researchers should use hybrid systems that rely on multiple, convergent natural language algorithms.     

Mirror neurons in humans: consisting or confounding evidence?

The widely known discovery of mirror neurons in macaques shows that premotor and parietal cortical areas are not only involved in executing one's own movement, but are also active when observing the action of others. The goal of this essay is to critically evaluate the substance of functional magnetic resonance imaging (fMRI) and positron emission tomography (PET) studies whose aim has been to reveal the presence of a parallel system in humans. An inspection of this literature suggests that there is relatively weak evidence for the existence of a circuit with 'mirror' properties in humans, such as that described in monkeys.     

Grey parrot numerical competence: a review

The extent to which humans and nonhumans share numerical competency is a matter of debate. Some researchers argue that nonhumans, lacking human language, possess only a simple understanding of small quantities, generally less than four. Animals that have, however, received some training in human communication systems might demonstrate abilities intermediate between those of untrained nonhumans and humans. Here I review data for a Grey parrot (Psittacus erithacus) that has been shown to quantify sets of up to and including six items (including heterogeneous subsets) using vocal English labels, to comprehend these labels fully, and to have a zero-like concept. Recent research demonstrates that he can also sum small quantities. His success shows that he understands number symbols as abstract representations of real-world collections, and that his sense of number compares favorably to that of chimpanzees and young human children.     

Grounding words in perception and action: computational insights

We use words to communicate about things and kinds of things, their properties, relations and actions. Researchers are now creating robotic and simulated systems that ground language in machine perception and action, mirroring human abilities. A new kind of computational model is emerging from this work that bridges the symbolic realm of language with the physical realm of real-world referents. It explains aspects of context-dependent shifts of word meaning that cannot easily be explained by purely symbolic models. An exciting implication for cognitive modeling is the use of grounded systems to 'step into the shoes' of humans by directly processing first-person-perspective sensory data, providing a new methodology for testing various hypotheses of situated communication and learning.