Action word meaning representations in cytoarchitectonically defined primary and premotor cortices

Abstract

Recent models of language comprehension have assumed a tight coupling between the semantic representations of action words and cortical motor areas. We combined functional MRI with cytoarchitectonically defined probabilistic maps of left hemisphere primary and premotor cortices to analyse responses of functionally delineated execution- and observation-related regions during comprehension of action word meanings associated with specific effectors (e.g., punch, bite or stomp) and processing of items with various levels of lexical information (non body part-related meanings, nonwords, and visual character strings). The comprehension of effector specific action word meanings did not elicit preferential activity corresponding to the somatotopic organisation of effectors in either primary or premotor cortex. However, generic action word meanings did show increased BOLD signal responses compared to all other classes of lexical stimuli in the pre-SMA. As expected, the majority of the BOLD responses elicited by the lexical stimuli were in association cortex adjacent to the motor areas. We contrast our results with those of previous studies reporting significant effects for only 1 or 2 effectors outside cytoarchitectonically defined motor regions and discuss the importance of controlling for potentially confounding lexical variables such as imageability. We conclude that there is no strong evidence for a somatotopic organisation of action word meaning representations and argue the pre-SMA might have a role in maintaining abstract representations of action words as instructional cues.

Introduction

It is now generally accepted that word meaning is represented in multiple areas of human cortex. This much was proposed by models of language comprehension in the mid-late nineteenth century. The classical Wernicke–Lichtheim model considered concepts to be distributed throughout the cerebral cortex, aroused by associations among speech perception and production related memory “images” in the left hemisphere superior temporal and inferior frontal cortices. As early as 1885, Lichtheim had proposed anatomically distributed and interconnected conceptual centres (see his Fig. 7; Compston, 2006, Smith, 1996), while Freud (1891) would later propose a distributed object concept system linked to word meanings (Henderson, 1992). Modern extensions and revisions of these early models continue to adhere to this precept, often making the additional assumption that representation of word meaning involves distributed networks of motor and somatosensory areas (e.g., Gallese and Lakoff, 2005, Martin and Chao, 2001, Tranel et al., 2001).

Some recent models of language comprehension have assumed a direct coupling between action meaning representations and cortical motor areas. One mechanism proposed to give rise to such a coupling is Hebbian learning, whereby “any two cells or systems of cells that are repeatedly active at the same time will tend to become ‘associated’, so that activity in one facilitates activity in the other” (Hebb, 1949, p. 70). Hence, the frequent co-presentation of an action word with the execution of the action the word refers to might result in a representation being associated with those motor areas (Pulvermüller, 1996, Pulvermüller, 2005). Alternatively, a class of visuomotor neurons in premotor cortex – mirror neurons – that respond congruently when an action is both observed and executed might serve to transform visual information into knowledge coded at an abstract level (Rizzolatti and Craighero, 2004). This mechanism might permit action knowledge to be retrieved by action related words (verbs).

Indirect evidence for cortical motor area involvement in action word meaning representation has been provided by transcranial magnetic stimulation (TMS), behavioural and neuroimaging studies. For example, several TMS studies have shown that processing of action related words and sentences is modulated by TMS-induced changes in excitability of left hemisphere cortical motor areas. During application of TMS, Pulvermüller et al. (2005) demonstrated faster lexical decisions to visually presented action words, while Buccino et al. (2005) noted responses slowed when participants listened to effector related action sentences. Oliveri et al., 2004, Buccino et al., 2005 reported, respectively, that motor evoked potentials (MEPs) recorded from effector muscles were enhanced or reduced when TMS was applied at long or short temporal intervals following action word presentation. Behavioural studies have also shown that action word processing can affect motor performance deleteriously when presented shortly after action onset  (< 200 ms; e.g., Boulenger et al., 2006). In order to explain these apparently contradictory facilitation and interference effects, Boulenger et al. (2006) have recently suggested the former could reflect post-lexical engagement of motor imagery mechanisms while the latter might be due to competition for common motor resources occurring during lexical access. More recently, Tomasino et al. (2008) reported that TMS applied at both long and short intervals following action word presentation facilitated motor responses when participants were instructed to imagine themselves performing the action, although not for simple reading or frequency judgement conditions.

Neuroimaging studies have provided relatively consistent evidence that retrieval of action word meanings activates cortical areas within the vicinity of the left precentral gyrus (e.g., Canessa et al., 2008, Rüschemeyer et al., 2007, Vigliocco et al., 2006; see Pulvermüller, 2005 for an overview of earlier work). A more precise localisation to actual motor areas has been suggested by several recent studies that attempted to link action word meaning representations (e.g., punch, stomp or bite) associated with specific effectors (i.e., hand, foot or mouth) to somatotopically organised motor areas (e.g., Aziz-Zadeh et al., 2006, Hauk et al., 2004, Tettamanti et al., 2005). In order to demonstrate a congruent somatotopic organisation of action meaning representations, two of these functional MRI studies first identified areas involved in action execution (Hauk et al., 2004) and observation (Aziz-Zadeh et al., 2006) within inferior frontal, precentral and middle frontal gyri according to the involvement of their related effectors. These functionally defined motor regions were then interrogated for activity during reading of effector related action words or sentences. These studies reported BOLD signal differences for comparisons between effector action words and a single control condition that were in some cases only indicative of a trend (e.g., effector pairwise comparisons at p < .1; e.g., Aziz-Zadeh et al., 2006) or only significant for two effectors when ROI overlap was the criterion (e.g., Hauk et al., 2004; see Kung et al. (2007) for a systematic critique of ROI overlap analyses). To our knowledge, no neuroimaging study has yet reported significant effects for all three effectors consistent with a complete somatotopic organisation.

Unfortunately, macrostructural features such as gyri and sulci tend not to be reliable indicators of cytoarchitectonic borders (Amunts et al., 2007). Premotor (PM) cortex in particular has no macroanatomical landmark to indicate the border between it and the prefrontal cortex anteriorly where more cognitive functions predominate (Geyer, 2003). Neuroimaging and stimulation studies have indicated a ventral to dorsal somatotopic organisation paralleling that of the primary motor cortex (area 4), and like the monkey (e.g., Godschalk et al., 1995), successive overlap of effector representations (Sanes and Schieber, 2001, Schubotz and von Cramon, 2003). However, unlike the lateral surface of monkey PM cortex, the dorsal (PMd) and ventral (PMv) sectors of area 6 in humans have no cytoarchitectonic features that might distinguish them (Picard and Strick, 1996). In addition, within the medial subdivision of PM cortex, the rostrally located pre-supplementary motor area (pre-SMA) shows little evidence of distinct effector related areas, and may instead support more abstract or cognitive functions, while the caudally situated SMA-proper has a clearer rostrocaudal somatotopic organisation (Picard and Strick, 1996).

Given the issues associated with localising responses accurately to motor areas in neuroimaging studies, we plotted the peak maxima reported by previous investigations in relation to cytoarchitectonic maximum probability maps (MPMs) of human primary and PM cortex derived from microcellular studies of post-mortem brains (i.e., areas 4 and 6; Eickhoff et al., 2006, Geyer, 2003). The MPM technique is robust to areal misclassifications of voxels and provides a “sufficient” coverage of the cytoarchitectonic volume (Eickhoff et al., 2006). We plotted relatively large 10 mm spheres around the peak maxima from these studies rather than their reported spatial extents as different thresholds or thresholding strategies used across studies result in activations of varying sizes (see Eickhoff et al., 2007). We reasoned that if action meaning representations are indeed organised somatotopically, then one would expect them to be located within the cytoarchitectonic borders of primary motor and PM cortex where motor somatotopy has been demonstrated by stimulation and neuroimaging studies. As can be seen from Fig. 1, this was not the case. In some instances, there was little agreement across studies for peaks reported for a given effector, an issue that we will discuss in more detail later (e.g., Aziz-Zadeh et al., 2006, Hauk et al., 2004, Tettamanti et al., 2005).

It is important to note that even if the activity reported by these studies had been located within the cytoarchitectonic MPMs, it would not constitute definitive proof that these areas mediate semantic representations of action words. An alternative interpretation is that this activity may reflect the by-product of imagery of an action (e.g., Jeannerod, 2001), emerging only following identification of the action concept and not being part of the representation of the action word per se (Willems and Hagoort, 2007). For example, Tomasino et al. (2007) reported motor cortical activity when their participants imagined the situation described in an action phrase, but not when they performed a secondary letter detection task designed to prevent imagery. In an attempt to minimise the influence of imagery, studies have typically administered the comprehension task first, followed by action execution (Hauk et al., 2004) or observation tasks (Aziz-Zadeh et al., 2006).

A more direct experimental control would be to include a condition involving imageable, concrete words. Comparisons to date have been between action word meanings and abstract word meanings (Aziz-Zadeh et al., 2006, Tettamanti et al., 2005) or visual character strings (Hauk et al., 2004), neither of which elicit comparable imagery. In order to control for motor imagery per se, action words would need to be employed as control stimuli, which would clearly introduce an experimental confound. However, a number of neuroimaging studies have reported that reading concrete words unrelated to motor function evokes activity in left hemisphere motor areas when contrasted with reading of less imageable abstract words (e.g., D'Esposito et al., 1997, Mellet et al., 1998, Pulvermüller and Hauk, 2006), indicating that they might prove adequate for eliciting generic imagery related activity in motor areas.

In the present study, we combined functional MRI with cytoarchitectonically defined probabilistic maps of primary and PM cortex to analyse the responses of both movement execution- and observation-related regions during retrieval of action word meanings associated with specific effectors. The use of both action observation and execution conditions to demonstrate overlapping activity is a necessary requirement for confirming the operation of mirror neurons (see Turella et al., 2008). It is worth noting that the neuroimaging studies cited in support of shared action word meaning comprehension and mirror neuron activity have tended to employ only action observation tasks (e.g., Aziz-Zadeh et al., 2006) or omitted action tasks altogether (e.g., Tettamanti et al., 2005). We also employed a range of conditions controlling for various levels of lexical information, including concrete words of equivalent imageability unrelated to body parts or actions, regular phonology (nonwords) and visual character recognition (hashes). This represents, to our knowledge, the first systematic attempt to test a proposed somatotopic organisation of action word meaning representations with fMRI.