With his massive redeployment hypothesis (MRH), Anderson proposes an attractive view of neural reuse by claiming that neural circuits initially dedicated to a specific function can be reused in the course of human evolution to support novel cognitive functions. Because this is meant to occur whenever a pre-existing circuit already possesses useful mechanisms for a novel function, Anderson's proposal challenges the assumption of concept empiricism that neural reuse is causally related to sensorimotor experience. Here, we question the idea that the mere availability of neural resources is sufficient to explain how new functions emerge from neural reuse, and we highlight the role of sensorimotor experience during the ontogenetical development of a new function by reviewing recent findings from studies in numerical cognition.

In the past few years, finger control and numerical cognition have been shown to share common areas in the parietal and premotor cortices (Andres et al. Reference Andres, Seron and Oliver2007; Pesenti et al. Reference Pesenti, Thioux, Seron and De Volder2000; Zago et al. Reference Zago, Pesenti, Mellet, Crivello, Mazoyer and Tzourio-Mazoyer2001). This common ground for finger movements and number processing may be a developmental trace of the use of fingers when learning to count (Butterworth Reference Butterworth1999a). In contrast, Anderson and colleagues (see Penner-Wilger & Anderson Reference Penner-Wilger, Anderson, Love, McRae and Sloutsky2008) propose that the neural network originally evolved for finger representation has been redeployed to serve numerical cognition only because it offers suitable resources to represent numbers, such as a register made of switches that can be independently activated. Accordingly, sensorimotor experience would play no role in the development of numerical cognition. However, a growing body of empirical data makes this perspective untenable. Indeed, finger use was found to deeply impact the acquisition of numerical skills in at least four different ways.

First, developmental studies indicate not only that children with poor abilities to discriminate their fingers are more likely to experience difficulties in mathematical tests (Fayol et al. Reference Fayol, Barrouillet and Marinthe1998; Noel Reference Noël2005), but also that an extensive training in finger differentiation, via sensorimotor exercises, improves both finger gnosis and numerical abilities (Garcia-Bafalluy & Noël Reference Garcia-Bafalluy and Noël2008). This shows that sensorimotor experience critically contributes to reaching an optimal performance during the acquisition of new numerical skills and, more generally, to making neural reuse effective in supporting new functions.

Second, a cross-cultural brain imaging study with participants from Eastern and Western cultures showed that cultural and educational habits can shape neural resources (Tang et al. Reference Tang, Zhang, Chen, Feng, Ji, Shen, Reiman and Liu2006). Various numerical tasks activated similar networks in occipito-parietal, perisylvian, and premotor areas in both cultures, but English participants showed higher activity in the perisylvian areas, whereas Chinese participants showed higher activity in premotor areas, a finding difficult to explain unless one considers their high level of practice in calculations with an abacus which requires a fine control of finger movements (Cantlon & Brannon Reference Cantlon and Brannon2007; Tang et al. Reference Tang, Zhang, Chen, Feng, Ji, Shen, Reiman and Liu2006). The cerebral network underlying numerical cognition can thus be shaped by the constraints that culture and/or education exert on the way individuals physically represent and manipulate numbers, thereby providing key evidence against the deterministic view conveyed by the MRH.

Third, even if Anderson's proposal makes it clear why pre-existing neural resources may underlie new representations, such as numbers, it remains confusing how these representations acquire their conceptual meanings. The idea that number semantics could also pre-exist in the brain is still disputed (see Rips et al. Reference Rips, Bloomfield and Asmuth2008; and our comment, Andres et al. Reference Andres, Di Luca and Pesenti2008). We argue that the use of finger counting can account for conceptual properties of numbers that are left undefined in the initial redeployment of pre-existing neural resources. For instance, the stable sequence of finger movements performed by children while counting, presumably under the combined influence of motor constraints and cultural habits, may lead them to understand that natural numbers include a unique first element, and that each number in a sequence has a unique immediate successor and a unique immediate predecessor, except the first (Wiese Reference Wiese2003). This suggests that neural reuse involves domain-structuring inheritance, as predicted by concept empiricism, but not by a strong version of the MRH.

Furthermore, the recurrent use of a stable finger-counting strategy during childhood keeps on influencing the way numbers are represented and processed in adults. Indeed, we recently showed that, when participants are asked to identify Arabic digits by pressing keys with their ten fingers, a finger-digit mapping congruent with their prototypical finger-counting strategy leads to a better performance than any other mapping, suggesting that number semantics of educated adults is grounded in their personal experience of finger counting (Di Luca et al. Reference Di Luca, Graná, Semenza, Seron and Pesenti2006). The finding that, in long-term memory, the structure of newly acquired concepts reflects idiosyncratic aspects of sensorimotor experience challenges Anderson's proposal that neural reuse anticipates concept formation. One may argue that neural redeployment may constrain or predispose individuals to count the way they do. However, this alternative explanation cannot account for the multiplicity of finger-counting strategies observed across individuals and cultures (Butterworth Reference Butterworth1999b; Wiese Reference Wiese2003). It is also incompatible with the results of an unconscious priming study showing that number semantics are linked not only to finger-counting, but also to finger-monitoring configurations (i.e., finger configurations used to show numerosities to other people; Di Luca & Pesenti Reference Di Luca and Pesenti2008).

Finally, recent findings show that object-directed actions mediate some aspects of the functional relationship between fingers and numbers. For example, observing grip closure movements interferes with numerical magnitude processing, suggesting the automatic activation of a magnitude code shared by numbers and finger movements (Badets & Pesenti Reference Badets and Pesenti2010). Critically, this interference is not observed when viewing non-biological closure movements, which suggests that it does not result from a general system for processing movement amplitude. This finding rather underlines the need to postulate a grounding mechanism, as predicted by empiricist accounts only.

In conclusion, although pre-existing circuits might be reused to provide representational resources for novel functions, we propose that these resources remain insufficient, and possibly unspecified, without the involvement of sensorimotor experience. In order to obtain a more universal theory of neural reuse, future studies now have to clarify how representational resources are shaped by cultural and educational constraints and how they interact with the functions they support.