The Two-Level Theory of verb meaning: An approach to integrating the semantics of action with the mirror neuron system
Introduction
Many traditional approaches to the human conceptual system assume that semantic knowledge is represented separately from, and is qualitatively different than, modality-specific systems for perception, action, and emotion (e.g., Barsalou and Hale, 1993, Fodor, 1975, Landauer and Dumais, 1997, Pylyshyn, 1984, Smith, 1978). According to this classic “disembodied cognition hypothesis” (Mahon & Caramazza, 2008), sensorimotor and affective representations are transduced into amodal structures such as feature lists, semantic networks, frames, etc., and cognitive processes operate on those structures, not on memories of the original experiences. Moreover, the content of all types of concepts, including those encoded by words, is believed to consist entirely of combinations of these abstract symbols.
A very different line of thinking is currently being pursued by a growing number of researchers in linguistics (e.g., Bergen, 2007, Evans and Green, 2006, Hampe, 2005), philosophy (e.g., Prinz, 2005, Gallagher, 2005, Johnson, 2007), psychology (e.g., Barsalou, 2008b, Gibbs, 2006, Pecher and Zwaan, 2005, Klatzky et al., 2008), and neuroscience (e.g., Barsalou, 2008a, Barsalou, 2008c, Haggard et al., 2007, Jeannerod, 2006, Kemmerer, in press, Keysers and Gazzola, 2006, Martin, 2007), all of whom endorse one form or another of what is often called the Embodied Cognition Framework (also known as the Grounded Cognition Framework or the Simulation Framework). The central tenet of this approach is that semantic knowledge is not purely amodal, but is instead anchored in modality-specific input/output systems, such that many forms of conceptual processing involve the transient recapitulation of diverse aspects of sensorimotor and affective experiences. As emphasized recently by Hoenig et al., 2008, Kemmerer, in press, the notion of modality-specific semantic maps does not rule out the possibility of higher-order integrative memory systems that contain systematically organized “conjunctive units” for binding cross-modal feature correlations; indeed, there is accumulating evidence that, at least for certain kinds of object concepts, integrative systems of this nature may reside in the temporal poles (e.g., Bright et al., 2007, Lambon Ralph et al., in press, Patterson et al., 2007). The most important, and most controversial, claim of the Embodied Cognition Framework, however, is that these integrative systems are not by themselves sufficient for full-fledged conceptual processing; rather, such processing requires that the abstract conjunctive units within the integrative systems activate, in top–down fashion, modality-specific representations that “flesh out”, to varying degrees, the contextually most appropriate concrete content of the relevant ideas (Damasio, 1989a, Damasio, 1989b, Damasio, 1989c, Simmons and Barsalou, 2003.
In recent years a great deal of research within the Embodied Cognition Framework has focused on the nature of action concepts, and this is due in large part to the seminal—some would even say “paradigm-shattering” (Ramachandran, 2008)—discovery of mirror neurons nearly 20 years ago (di Pellegrino, Fadiga, Fogassi, Gallese, & Rizzolatti, 1992). These are cells that discharge not only when certain kinds of actions are executed by the self, but also when they are seen or heard being performed by someone else. Thus, mirror neurons appear to represent behavioral patterns per se, and because they neutralize the self–other distinction,1 they may turn out to have profound implications for intersubjective understanding (Hurley, 2008, Iacoboni, 2008). Owing to their remarkable response properties, these cells seem to confirm a prescient statement made by an early advocate of the Embodied Cognition Framework, namely William James (1890, p. 526): “Every representation of a movement awakens in some degree the actual movement which is its object”.
Mirror neurons have been found in a variety of brain regions, but before briefly reviewing those results we would first like to clarify our terminology. There is currently some disagreement over the definition of “mirror neurons”. Cells that fire during both action execution and action observation were first discovered in area F5 of the macaque ventral premotor cortex, and this region has continued to received a great deal of attention over the years. Apparently for this purely historical reason, however, some researchers seem to think that only F5 cells deserve to be called “mirror neurons”, and that cells in other cortical areas that also fire during both action execution and action observation do not qualify. For example, after providing compelling evidence that cells with mirror-like properties—i.e., cells that achieve action observation-execution matching—are broadly distributed across many sectors of the macaque frontal cortex, Raos, Evangeliou, and Savaki (2007, p. 12682) conclude that their results “undermine the ‘mirror neuron system’ concept”, and that the more general notion of “mental simulation” is explanatorily superior because it, rather than the former concept, “assigns the role of understanding others’ actions to the entire distributed neural network, which is responsible for the execution of actions”. The same research team recently expressed essentially the same view after extending their work to multiple sectors of the macaque parietal cortex (Evangeliou, Raos, Galletti, & Savaki, in press). We believe, however, that “mirror neurons” should be defined by functional rather than anatomical criteria. Indeed, this perspective is adopted in several prominent reviews of the mirror neuron system which indicate that the system is not necessarily limited to F5 (Rizzolatti and Craighero, 2004, Rizzolatti et al., 2001).
Having said that, we consider it noteworthy that in the macaque brain mirror neurons have already been found in an impressively large number of areas:
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ventral premotor cortex (di Pellegrino et al., 1992, Ferrari et al., 2003, Gallese et al., 1996, Keysers et al., 2003, Kohler et al., 2002, Nelissen et al., 2005, Raos et al., 2007, Rizzolatti et al., 1996);
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dorsal premotor cortex (Cisek and Kalaska, 2004, Raos et al., 2007);
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primary motor cortex (Raos et al., 2004, Raos et al., 2007, Tkach et al., 2007);
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several medial frontal regions (Raos et al., 2007);
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inferior parietal cortex (Fogassi et al., 2005, Gallese et al., 2002, Evangeliou et al., in press);
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superior parietal cortex (Evangeliou et al., in press);
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primary and supplementary somatosensory areas (Evangeliou et al., in press).
There is mounting evidence that mirror neurons also exist in a wide range of human brain areas. Despite some important limitations that we address later (Mahon and Caramazza, 2005, Mahon and Caramazza, 2008, Negri et al., 2007, Turella et al., 2009), numerous human brain mapping studies suggest that the visual or auditory perception of an action engages many of the same neural networks that are recruited during its execution—a remarkable phenomenon which suggests that understanding other people’s actions may involve, to some degree, simulating them in a completely automatic, unconscious manner (we discuss some of this literature in Sections 3.1 Mirror neurons, 4.1 Mirror Neurons).
In addition, a growing literature suggests that, as predicted by the Embodied Cognition Framework, when people understand linguistic descriptions of actions, motor-related regions in their frontal lobes are engaged (for reviews see Fischer and Zwaan, 2008, Pulvermüller, 2005, Pulvermüller, 2008, Willems and Hagoort, 2007). So far, linguistically triggered motor resonance has not been investigated in as much detail as the type of motor resonance that is induced by action observation, but there is increasing interest in the provocative idea that comprehending a linguistic description of an action might involve covertly recapitulating the type of action that it refers to, using some of the same brain systems that underlie the execution and observation of that type of action. As yet, however, this line of research has, for the most part, neglected recent advances in linguistic theory, especially regarding the lexical and grammatical encoding of action. The main purpose of this paper is therefore to take some steps toward filling that gap.
In particular, our aim is to explore some possible connections between, on the one hand, the Embodied Cognition Framework as it has hitherto been applied to action concepts and the mirror neuron system, and on the other hand, the Two-Level Theory of verb meaning, which is an approach to analyzing the linguistic representation of action that has not only been supported and refined for over 20 years (for a review see Levin & Rappaport Hovav, 2005), but has also arguably led to deep insights about the fabric of human thought (Pinker, 2007). Basically, the Two-Level Theory holds that verb meanings have two separate levels of structure—one for the “root” or “constant” semantic features that characterize individual verbs, and another for the “event structure templates” or “thematic cores” that are shared by all the verbs in a given class. In Section 2 we elaborate this central claim of the theory in greater detail. Then in Sections 3 Hypothesis 1: Root-level motor features of verb meaning are partially subserved by somatotopically mapped mirror neurons in the left primary motor and/or premotor cortices, 4 Hypothesis 2: Template-level motor features of verb meaning are partially subserved by representationally schematic mirror neurons in Brodmann area 44 of the left inferior frontal gyrus we explore the following hypotheses about how, with specific reference to the motor features of action verbs, the two distinct levels of semantic representation might correspond to two distinct levels of the mirror neuron system:
Hypothesis 1. Root-level motor features of verb meaning are partially subserved by somatotopically mapped mirror neurons in the left primary motor and/or premotor cortices.
Hypothesis 2. Template-level motor features of verb meaning are partially subserved by representationally more schematic mirror neurons in Brodmann area (BA) 44 of the left inferior frontal gyrus.
We have deliberately shaped these hypotheses in the form of rather bold proposals about how the semantics of action might relate to the mirror system, because our intent is to provide some intriguing theoretical ideas around which both past and future research can be organized. We show that evidence has been accumulating in support of the general neuroanatomical claims made by both hypotheses—namely, that each level of verb meaning is associated with the designated cortical areas. However, we also point out a number of problems, the most important of which is that, to the best of our knowledge, as yet no studies have satisfied all the criteria necessary to support the more specific neurobiological claims made by the two hypotheses—namely, that each level of verb meaning is associated with mirror neurons in the pertinent brain regions. Strictly speaking, such studies would need to demonstrate that within those brain regions overlapping neuronal populations, and ultimately the very same cells (Dinstein, Thomas, Behrmann, & Heeger, 2008), are functionally engaged during all three of the following conditions: (a) the linguistic processing of particular motor features of verb meaning, (b) the execution of actions with the corresponding motor features, and (c) the observation of actions with the corresponding motor features. We suggest several ways in which the Two-Level Theory could help guide future research aimed at evaluating and refining Hypotheses 1 and 2.
Before proceeding, a caveat is in order. Our hypotheses focus rather narrowly on how certain aspects of verb meaning might be linked with mirror neurons in certain regions of the left frontal lobe. The main reason we restricted the hypotheses in these ways is because we felt it necessary to constrain the scope and length of the paper. We would like to point out, however, that even though the hypotheses do not directly address parietal and temporal brain regions, we consider it likely that some of those regions also contribute, in various ways, to the linguistic representation of action. In fact, several recent studies point to the presence of mirror neurons in the left intraparietal sulcus and inferior parietal lobule (e.g., Dinstein et al., 2007, Hamilton and Grafton, 2006, Hamilton and Grafton, 2007, Hamilton and Grafton, 2008, Shmuelof and Zohary, 2006), and there is growing evidence that these same regions also support some aspects of verb meaning (e.g., Kemmerer et al., 2008, Noppeney et al., 2005, Saccuman et al., 2006, Tranel et al., 2008). While investigating possible relations between mirror neurons and verb meanings in the left parietal cortex is beyond the purview of this paper, it is clearly an important direction for future research (e.g., see Glenberg & Gallese, submitted for publication, for a new theoretical proposal about the role of action-related frontoparietal circuits in sentence processing). In addition, our hypotheses do not encompass the posterolateral temporal cortex, despite the fact that this region plays a major role, albeit predominantly in the right hemisphere, in biological motion perception (for a review see Blake & Shiffrar, 2007) and has also been implicated, albeit predominantly in the left hemisphere, in the semantic processing of action verbs (e.g., Kable et al., 2002, Kable et al., 2005, Kemmerer et al., 2008, Noppeney et al., 2005, Pirog Revill et al., 2008, Tranel et al., 2008; see also relevant data on thematic roles and event structure provided by, e.g., Bedny. et al., in press, Grewe et al., 2007, Wu et al., 2007). We would like to emphasize, however, that even though we do not discuss the posterolateral temporal cortex in detail, we nevertheless refer, at several points in our presentation, to findings about this region that are especially pertinent to our arguments (see in particular Sections 3.2.2.1 Activation patterns, 4.2.2.2 Lesion studies).
Section snippets
The theory in a nutshell
The Two-Level Theory subsumes a number of complex, well-developed proposals about the linguistic representation of action. These proposals differ in non-trivial ways, but as noted above, all of them share the fundamental assumption that the meanings of verbs have two separate levels of semantic structure (for a brief overview of this research see Levin & Rappaport Hovav, in press; for a broader survey see Levin & Rappaport Hovav, 2005; see also Bornkessel et al., 2006, Croft, 1991, Croft, 1998,
Hypothesis 1: Root-level motor features of verb meaning are partially subserved by somatotopically mapped mirror neurons in the left primary motor and/or premotor cortices
In this section we approach Hypothesis 1 in the following way. First, we describe the somatotopic organization of the primary motor and premotor cortices, and we briefly review evidence that these regions contain mirror neurons that mediate action observation-execution matching in an effector-congruent fashion. Second, we consider the question of whether these mirror neurons also contribute to representing root-level motor features of the meanings of action verbs, such as the kinematic
Hypothesis 2: Template-level motor features of verb meaning are partially subserved by representationally schematic mirror neurons in Brodmann area 44 of the left inferior frontal gyrus
We turn now to Hypothesis 2. First, we describe a special category of mirror neurons that mediate action observation-execution matching in a way that focuses on the goals and intentions, rather than the manners, of object-directed movements. Cells with these relatively abstract tunings have been identified in area F5 of the macaque ventral premotor cortex, and there is mounting evidence that they also exist in the putative human homologue of that region, namely BA44 of the inferior frontal
Conclusion
We have explored the possibility that two separate levels of verb meaning map onto two separate levels of the mirror neuron system. Hypothesis 1 holds that root-level motor features of verb meaning depend on somatotopically organized mirror neurons in the left primary motor and/or premotor cortices. Hypothesis 2 holds that template-level motor features of verb meaning depend of representationally more schematic mirror neurons in BA44 or the left inferior frontal gyrus. Evidence has been
Acknowledgments
For statistical advice we thank Tom Talavage, and for generous comments on previous versions of the paper we thank Arthur Glenberg, Natalya Kaganovich, Gina Kuperberg, Nathan Lautz, Brad Mahon, Evie Malaia, Megan MacPherson, Luke Miller, Steve Pinker, Friedemann Pulvermüller, Mikkel Wallentin, Ronnie Wilbur, and Rolf Zwaan. We are especially grateful to Greig de Zubicaray, Anjan Chatterjee, and Eileen Cardillo for providing very detailed and constructive feedback. Needless to say, we alone are
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