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Aphasia, Apraxia and the Evolution of the Language-Ready Brain

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Aphasia, Apraxia and the Evolution of the Language-Ready Brain APHASIOLOGY, 2006, 20 (9/10/11), 1125–1155 Aphasia, apraxia and the evolution of the language-ready brain Michael A. Arbib University of Southern California, Los Angeles, CA, USA Background: The Mirror System Hypothesis offers the mirror system for grasping (i.e., neural mechanisms active for both execution and observation of grasping) as a neural ‘‘missing link’’ between the brains of our non-human ancestors of 20 million years ago and the modern human language-ready brain, stressing the importance of manual gesture in the evolution of mechanisms supporting language. Aims: To assess the view that neural mechanisms for both praxis and language share an evolutionary relationship to the ancestral mirror system for grasping. Main Contribution: The praxis system receives a new analysis based on the attempt to link human praxis to computational models of execution and observation of grasping in the macaque as well as the analysis of parallels between language and praxis. Conclusions: The conceptual analysis presented here may prove insightful for clinicians seeking to relate and differentiate aphasia and apraxia. Since humans can learn language and monkeys and chimpanzees cannot, we seek brain regions that are homologous across these species (i.e., there is evidence for a shared ancestry) so that we may infer from analysis of both their similarities and differences what might have been the brain architecture of our common ancestor, and what may have changed along our varied evolutionary paths. The present discussion is rooted in the homology between human Broca’s area, traditionally thought of as a speech area, and premotor area F5 of the macaque brain (Rizzolatti & Arbib, 1998). But first some definitions: Address correspondence to: Michael A. Arbib, Computer Science Department, Neuroscience Program, and USC Brain Project, University of Southern California, Los Angeles, CA 90089-2520, USA. E-mail: [email protected]; web page: http://www-hbp.usc.edu/). This work was supported in part by NIH under grant 1 P20 RR020700-01 to the USC/UT Center for the Interdisciplinary Study of Neuroplasticity and Stroke Rehabilitation (ISNSR). In addition to thanking John Marshall, David Caplan, and Giacomo Rizzolatti for their early stimulus to my research on computational neurolinguistics and then the mirror system hypothesis, I want particularly to thank Anna Barrett, Anne Foundas, and Kenneth Heilman for the critique of the hypothesis that laid down the gauntlet that the present article picks up, and Chris Code, Laurel Buxbaum, Scott Frey, Rafaella Rumiati, and Angela Sirigu for guiding me through a number of relevant intricacies of the literature on apraxia and aphasia. # 2006 Psychology Press Ltd http://www.psypress.com/aphasiology DOI: 10.1080/02687030600741683 1126 ARBIB 1. A mirror neuron for an action x is a neuron that is active in the brain of an animal both when that animal executes an action of type x and when it observes another animal execute an action of type x. 2. However, this does not imply that such a neuron of itself encodes action x; for example, the neuron might encode a feature of action x (whether of the movement performed during action x, or the goal to which x is directed, or both) and thus be part of a population code for x or some other process associated with x. 3. A mirror system for a class X of actions is a region of the brain that, compared with other situations, becomes more active both when actions from class X are observed and when actions from class X are executed. Neurophysiological studies have shown mirror neurons for a wide range of actions in the macaque monkey, and brain-imaging experiments have demonstrated a mirror system for grasping in the human, but we have no single neuron studies proving the reasonable hypothesis that the human mirror system for grasping contains mirror neurons for specific grasps. More specifically, area F5 (the fifth region in a numbering for areas of the macaque frontal lobe) in ventral premotor cortex contains, among other neurons, a set of neurons that fire when the monkey executes a specific manual action (e.g., one neuron might fire when the monkey performs a precision pinch, another might fire when the monkey executes a power grasp). A subset of these neurons, the so-called mirror neurons, also discharge when the monkey observes meaningful hand movements made by the experimenter which are similar to those whose execution is associated with the firing of the neuron (Rizzolatti, Fadiga, Gallese, & Fogassi, 1996). By contrast, the canonical neurons are those belonging to the complementary, anatomically segregated subset of grasp-related F5 neurons that fire when the monkey performs a specific action but not when it observes a similar action. We further stress that mirror neurons for grasping have also been found in parietal areas of the macaque brain. Moreover, brain-imaging studies demonstrate that there are mirror systems for grasping (i.e., regions active for both observation and execution of grasping) in Broca’s area and parietal cortex. (For more information on the anatomy and neurophysiology, see Rizzolatti, Luppino, & Matelli, 1998; and Rizzolatti, Fogassi & Gallese, 2001). These findings are the basis for: N The Mirror System Hypothesis (MSH): The parity requirement for language in humans—that what counts for the ‘‘communicator’’ [e.g., speaker] must count approximately the same for the ‘‘communicatee’’ [e.g. hearer]—is met because Broca’s area evolved atop the mirror system for grasping with its capacity to generate and recognise a set of actions. Here, hand and face gestures may be used as well as, or instead of, vocal gestures for communication (Arbib & Rizzolatti, 1997; Rizzolatti & Arbib, 1998). When we explore the relation between praxis and communication, we will ask whether the same mirror neurons—accepting the hypothesis of (3)—are involved in both functions. Whether the answer is yes or no, it will be worth stressing that we must go ‘‘beyond the mirror’’—it is not mirror neurons alone that serve the various functions that interest us, but rather the larger systems (whose delimitation is a challenging task for present and future research) of which they form part. Although this article is not based on the work of John Marshall, its roots can in part be traced back to his influence and generosity. One morning in 1976, shortly EVOLUTION OF THE LANGUAGE-READY BRAIN 1127 after my family and I arrived in Edinburgh for a year’s sabbatical, there came a ring at the doorbell and there on the doorstep stood John Marshall, arriving unheralded to welcome us to Edinburgh. The friendship and conversations of the following year contributed to a rekindled interest in neurolinguistics that laid the basis for the paper by Arbib and Caplan (1979) and the two subsequent workshops at the University of Massachusetts at Amherst that eventually led to the book edited by Arbib, Caplan, and Marshall (1982); related efforts yielded the book by Arbib, Conklin, and Hill (1987). After that, my work on language entered a dormant stage but my work on brain mechanisms for the visual control of action proceeded apace, yielding among other things a partnership with Marc Jeannerod, Giacomo Rizzolatti, and Hideo Sakata (see Jeannerod, Arbib, Rizzolatti, & Sakata, 1995, for one result) that spanned the discovery of macaque mirror neurons in Parma and the linkage to Broca’s area that provided the foundation for MSH. Arbib (2005a) gives a comprehensive review of the current state of MSH, stressing that the formulation offered above is just a starting point for more detailed analysis. That review is accompanied by numerous commentaries and the author’s response. Of particular concern here is the commentary by Barrett, Foundas, and Heilman (2005) who discuss functional and structural evidence supporting differential localisation of the neuronal modules controlling limb praxis, speech and language, and emotional communication. They argue that such data rule against MSH. This paper will advance the debate, seeking to refute elements of their critique while conceding that definitive arguments in favour of MSH are still not available. EVOLUTIONARY PARCELLATION OF THE BRAIN As background for what follows, it will be useful to recall some key ideas from comparative neurobiology on the evolutionary parcellation of the brain. Butler and Hodos (1996) show that the course of brain evolution among vertebrates has been determined in great part by (a) formation of multiple new nuclei through elaboration or duplication; (b) regionally specific increases in cell proliferation in different parts of the brain; and (c) gain of some new connections and loss of some established connections. Increases in the overall size of mammalian neocortex are paralleled by increases in the number of its functional subdivisions and the complexity of the internal organisation of the subdivisions, although the differences between primates and other mammals, and between humans and other primates, appear to involve specific changes in circuitry beyond those related to the general sequelae of increase in brain size (Striedter, 2004, Chapter 9). Kaas (1993) and Krubitzer (1998) offer a detailed perspective on the evolution of cerebral cortex. The neocortex in mammals is divided into many functional subunits, each with a distinct variation on cortical cellular architecture and a unique pattern of connections. New cortical fields might be created by novel combinations of inputs, yielding new functions through varied processing of the patterns of activity in the inputs. Modules could then form within a field that are specialised for a given novel process (with these modules dispersed across the brain region to sample diverse parts of the input manifold). These modules might be of various column-like, band-like, or dot-like shapes, or even form layers or sublayers. Examples include the ocular dominance bands that subdivide primary visual cortex of some monkeys, cytochrome oxidase blob and interblob regions of primary cortex of primates, and 1128 ARBIB the irregular bands of cortex related to slowly adapting and rapidly adapting cutaneous receptors in SI of monkeys.
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