ABSTRACT
In this study, we addressed the issue of whether the brain sensorimotor circuitry that controls action production is causally involved in representing and processing action-related concepts. We examined the three-year pattern of evolution of brain atrophy, action production disorders, and action-related concept processing in a patient (J.R.) diagnosed with corticobasal degeneration. During the period of investigation, J.R. presented with increasing action production disorders resulting from increasing bilateral atrophy in cortical and subcortical regions involved in the sensorimotor control of actions (notably, the superior parietal cortex, the primary motor and premotor cortex, the inferior frontal gyrus, and the basal ganglia). In contrast, the patient's performance in processing action-related concepts remained intact during the same period. This finding indicated that action concept processing hinges on cognitive and neural resources that are mostly distinct from those underlying the sensorimotor control of actions.
Acknowledgements
We are very grateful to J.R. for his generous collaboration. We thank Adrian Ivanoiu from the Cliniques universitaires Saint-Luc, Brussels, for having referred the patient to us. Thanks also to Cecile Grandin who helped in reading the magnetic resonance images of J.R.
Disclosure statement
No potential conflict of interest was reported by the authors.
Notes
1. We do not mention here evidence from neuroimaging, neurophysiological, and behavioural studies demonstrating that motor processes are automatically activated when actions or manipulable objects or words referring to them are processed in tasks that do not envolve any intention to act (see for reviews, Aziz-Zadeh & Damasio, Citation2008; Culham & Valyear, Citation2006; Fischer & Zwaan, Citation2008; Lewis, Citation2006; Watson, Cardillo, Ianni, & Chatterjee, Citation2013; Willems & Hagoort, Citation2007). As it is now widely acknowledged, whereas such evidence supports the view that motor processes are automatically engaged when action concepts are retrieved, it does not constitute evidence that motor processing is constitutive of concept processing (e.g., Chatterjee, Citation2010; Csibra, Citation2007; Hauk & Tschentscher, Citation2013; Hickok, Citation2009; Kiefer & Barsalou, Citation2013; Mahon & Caramazza, Citation2008; Vannuscorps et al., Citation2013, Citation2014).
2. In a number of reports (e.g., Albani et al., Citation2010; Bertella et al., Citation2002; Cotelli et al., Citation2006; Pignatti et al., Citation2006; Spatt et al., Citation2002; Silveri & Ciccarelli, Citation2007; Stamenova et al., Citation2011), it was even unclear whether the deficit was specific to action pictures or verbs, because no data were provided about the patients’ performance with matched sets of non-action-related stimuli like animals, plants, or non-manipulable objects. Moreover, in most reports, it was not established whether the deficit was conceptual in nature, affecting specifically actions as a conceptual category, or was caused by the lexical retrieval of verbs, as a grammatical category of words, being impaired (see for discussion, Pillon & d'Honincthun, Citation2010).
3. In addition, we had included word/picture verification tasks in the protocol of investigation. We did so in order to be able to determine whether a naming deficit, if present, was due to an impairment at the word production level or at the conceptual level of processing entailed in the naming task. Because no naming deficit was observed in J.R. whatever the set of stimuli or the period of assessment, and since the word–picture verification task is known to be less sensitive for detecting a mild/moderate conceptual impairment than the naming task, we decided not to report here the results of the word/picture verification tasks, for the sake of brevity. Needless to say, the results obtained in the word-picture verification tasks led to the same conclusions as those drawn from the naming tasks.
4. Initially, the task was composed of 24 manipulable objects but 2 objects were discarded because the 3 judges disagreed about their manipulability.
5. However, in 28% of the trials, the same picture served as the target response for both the “gesture” and the “function” conditions, the two other pictures in the array being two visually related foils. These trials were included in order to discourage the participants from discarding the picture they had chosen in the first presentation of the probe when they were presented with it the second time.
6. G.C.’s pattern of recovery over time could only be inferred a posteriori. Of course, further studies focusing on the follow-up of functional recovery across domains after a stroke are needed.
7. Also, we would like to make clear that our conclusion does not concern other issues that are related but (in our opinion) should be treated as independent from that issue, like the organization of conceptual knowledge in the brain (e.g., Binder, Desai, Graves, & Conant, Citation2009; Caramazza & Shelton, Citation1998; Patterson, Nestor, & Rogers, Citation2007) and the modality-specific versus amodal nature of conceptual representations (e.g., Barsalou, Citation1999; Machery, Citation2007; Mahon & Caramazza, Citation2008). Thus, for example, our findings are not inconsistent with the view that the organization of conceptual knowledge in the brain is driven by the sensory and motor processing channels (e.g., Warrington & Shallice, Citation1984) and, in particular, with the proposal that the neural substrates underpinning action control and action conceptual processing are adjacent (Martin, Citation2007). They do, however, contradict the view that both kinds of processes depend on the same neural circuitry.
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Funding
This research was supported by the Fonds de la Recherche Scientifique – FNRS (F.R.S.-FNRS) [grant number 1.5192.10F to Agnesa Pillon].
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