Neural reuse is the notion that new cognitive skills are comprised of recombined and reused neural solutions, rather than independently evolved modules. In Anderson's version of such theories, the “massive redeployment hypothesis” (MRH), he predicts that newer cognitive functions will be more scattered across the brain. His reasoning is that local neural circuits have fixed internal workings across evolutionary time, which enables solutions to newer evolutionary problems to draw upon a more widely spread out set of neural building blocks. By providing evidence that all cognitive domains overlap and are distributed across the brain, Anderson convincingly negates the need for implementation of cognitive functions as sets of independently evolved, localized modules in the brain, and, at the same time, makes a compelling case for neural reuse. In our view, however, the MRH falls short of providing a full evolutionary-developmental explanation of brain organization because the roles of ontogenetic change and plasticity across the life span are overlooked.

In fact, one of the strongest lines of evidence against modular organization in the brain comes from in-depth analyses of developmental disorders across ontogeny. Although impairments in developmental disorders seem to be specific to particular cognitive domains and are often taken as evidence for innately specified modularity, this turns out not to be the case. On closer inspection, claims about intact and impaired cognitive modules have consistently overlooked subtle deficits in “intact” domains and have failed to trace cognitive-level impairments in the phenotypic outcome back to their basic-level origins in infancy; that is, they do not account for the full atypical cognitive spectrum over developmental time (see discussions in Karmiloff-Smith Reference Karmiloff-Smith1998; Reference Karmiloff-Smith2009; Southgate & Hamilton Reference Southgate and Hamilton2008).

Take, for example, the case of Williams syndrome (WS), caused by a hemizygous deletion of genes on chromosome 7, resulting in decreased expression of affected gene products throughout the brain from conception onwards. Although the effects of the deletion may be superficially more apparent in certain cognitive domains, in fact they turn out to be widespread across the multiple cortical regions where the genes are expressed and are therefore highly unlikely to be specific to single domain-specific modules. Indeed, in WS, impairments across several domains such as face processing, number, auditory and spatial perception (Brown et al. Reference Brown, Johnson, Paterson, Gilmore, Gsödl, Longhi and Karmiloff-Smith2003; Elsabbagh et al., in press; Paterson et al. Reference Paterson, Brown, Gsodl, Johnson and Karmiloff-Smith1999; Van Herwegen et al. Reference Van Herwegen, Ansari, Xu and Karmiloff-Smith2008) can be traced to a featural processing bias in infancy (Karmiloff-Smith et al. Reference Karmiloff-Smith, Thomas, Annaz, Humphreys, Ewing, Brace, van Duuren, Pike, Grice and Campbell2004), which itself is likely to be due to very early atypical saccadic eye movement planning (Karmiloff-Smith Reference Karmiloff-Smith2009). Theories that explain WS in terms of intact and impaired, innately specified modules are based on static descriptions of the phenotypic end state (Bellugi et al. Reference Bellugi, Lichtenberger, Mills, Galaburda and Korenberg1999; Pinker 1994; Rossen et al. Reference Rossen, Klima, Bellugi, Bihrle, Jones, Beitchman, Cohen, Konstantareas and Tannock1996), ignoring the complex dynamics of development. In contrast to modular theories of the brain, theories of neural reuse are far more likely to explain why pure cognitive deficits in specific brain regions have been so difficult to identify.

How the massive redeployment theory of neural reuse could give rise to adult-like brain organization across the life span needs to be specified further, however. Firstly, it remains unclear whether Anderson considers locally fixed internal workings to be already present at birth – in which case one innately specified mechanism (modules) is simply being replaced by another (fixed internal neuronal workings) – or whether his approach encompasses the development of such neural functions over ontogeny. On the one hand, aspects of neuronal differentiation may indeed emerge early in development through intrinsic factors that determine cortical connections, causing cortically localized functions to be highly preserved across individuals, cultures, and even species (but see Han & Northoff Reference Han and Northoff2008; Orban et al. Reference Orban, Van Essen and Vanduffel2004). On the other hand, research on brain plasticity shows that developmental pressures can dramatically reshape the inner workings of neurons. Most strikingly, this is illustrated by classic studies in which developing patches of cortex received abnormal sensory input. For example, when ferret auditory cortex neurons were rewired to receive visual input, and visual cortex neurons to receive auditory input, the inner workings of both types of neurons changed. The auditory cortex took on characteristics and assumed functions of the visual cortex and vice versa (von Melchner et al. Reference von Melchner, Pallas and Sur2000). A neuroconstructivist approach to brain development reconciles these two apparently contradicting sets of findings by suggesting that early differentiation may render certain parts of the cortex more relevant to performing certain functions. However, these initial systems are coarsely coded, and competition between regions gradually settles which regions with domain-relevant biases become domain-specific over time, ultimately giving rise to the structured adult brain (e.g., Johnson Reference Johnson2001; Karmiloff-Smith Reference Karmiloff-Smith1998; Reference Karmiloff-Smith2009).

A second issue that remains unclear is whether recombination of connections between specialized regions is the only mechanism that Anderson considers relevant, leaving no role for localized plasticity of neural computation in response to newly learnt tasks such as mathematics and reading. Dehaene's neuronal recycling hypothesis (Reference Dehaene, Dehaene, Duhamel, Hauser and Rizolatti2005) proposes that such culturally transmitted skills invade neural systems that are already present and that lend themselves well to performing these new tasks. If there is any difference between functions, optimizing a neural circuit with an existing function for a new task will consequently affect tasks that already relied on the same circuit. It remains unclear whether Anderson accepts this possibility or whether he maintains that inner neuronal workings are truly fixed, which would imply that learning a new task (e.g., reading) should never adversely affect other tasks that depend on the shared neuronal circuitry (e.g., object processing).

To summarize, we maintain that the consideration of ontogenetic change and developmental disorders can provide vital evidence for the organizational principles of the brain, principles that run counter to modular views. We agree with Anderson that neural reuse is a promising organizing principle of the brain, as opposed to the notion that the brain has evolved into a Swiss army knife with innately specified modules uniquely designed for each new cognitive function. However, we suggest that Anderson's massive redeployment hypothesis could be further constrained by considering brain development across ontogeny in order to provide a full evolutionary-developmental theory of neural reuse that encompasses both typical and atypical development.