An emerging class of theories concerning the functional structure of the brain takes the reuse of neural circuitry for various cognitive purposes to be a central organizational principle. According to these theories, it is quite common for neural circuits established for one purpose to be exapted (exploited, recycled, redeployed) during evolution or normal development, and be put to different uses, often without losing their original functions. Neural reuse theories thus differ from the usual understanding of the role of neural plasticity (which is, after all, a kind of reuse) in brain organization along the following lines: According to neural reuse, circuits can continue to acquire new uses after an initial or original function is established; the acquisition of new uses need not involve unusual circumstances such as injury or loss of established function; and the acquisition of a new use need not involve (much) local change to circuit structure (e.g., it might involve only the establishment of functional connections to new neural partners). Thus, neural reuse theories offer a distinct perspective on several topics of general interest, such as: the evolution and development of the brain, including (for instance) the evolutionary-developmental pathway supporting primate tool use and human language; the degree of modularity in brain organization; the degree of localization of cognitive function; and the cortical parcellation problem and the prospects (and proper methods to employ) for function to structure mapping. The idea also has some practical implications in the areas of rehabilitative medicine and machine interface design.

Simple specialization cannot account for brain functioning. Yet, we believe Anderson's reuse can be better explained by re-function. We suggest that functional demands shape brain changes and are the driving force behind reuse. For example, we suggest that the prefrontal cortex (PFC) is built as an infrastructure for multi-functions rather than as a module for reuse.

Mere physical experiences of warmth, distance, hardness, and roughness are found to activate the more abstract psychological concepts that are analogically related to them, such as interpersonal warmth and emotional distance, thereby influencing social judgments and interpersonal behavior without the individual's awareness. These findings further support the principle of neural reuse in the development and operation of higher mental processes.

Neural reuse theories suggest that, in the course of evolution, a brain structure may acquire or lose a number of cognitive uses while maintaining its cognitive workings (or low-level operations) fixed. This, in turn, suggests that homologous structures may have very different cognitive uses, while sharing the same workings. And this, essentially, is homology thinking applied to brain function.

Both distributed coding, with its implication of neural reuse, and more specialized function have been recognized since the beginning of brain science. A controversy over imageless thought threw introspection into disrepute as a scientific method, making more objective methods dominate. It is known in information science that one element, such as a bit in a computer, can participate in coding many independent states; in this commentary, an example is given.

Anderson suggests that theories of sensorimotor grounding are too narrow to account for his findings of widespread “reuse” supporting multiple different cognitive “task domains.” I call some of the methodological assumptions underlying this conclusion into question, and suggest that his examples reaffirm rather than undermine the special status of sensorimotor processes in cognitive evolution.

The compelling case that Anderson makes for neural reuse and against modularity as organizing principle of the brain is further supported by evidence from developmental disorders. However, to provide a full evolutionary-developmental theory of neural reuse that encompasses both typical and atypical development, Anderson's “massive redeployment hypothesis” (MRH) could be further constrained by considering brain development across ontogeny.

We isolate some critical aspects of the reuse notion in Anderson's massive redeployment hypothesis (MRH). We notice that the actual rearranging of local neural circuits at a timescale comparable with the reactivity timescale of the organism is left open. We propose the concept of programmable neural network as a solution.

Neural reuse posits development of functional overlap in brain system circuits to accommodate complex evolutionary functions. Evolutionary adaptation evolved neural circuits that have been exploited for many uses. One such use is engaging cognitive processes in memory consolidation during the neurobiological states of sleep. Neural reuse, therefore, should not be limited to neural circuitry, but be extended to include sleep-state associated memory processes.

We taxonomize the varieties of representational reuse and point out that all the sorts of reuse that the brain engages in (1) involve something like a model (or schema or simulator), and (2) are effected in bodily and external media, as well as neural media. This suggests that the real fundamental organizational principle is not neural reuse, but model reuse.

We argue that Anderson's “massive redeployment hypothesis” (MRH) needs further development in several directions. First, a thoroughgoing criticism of the several “embodied cognition” alternatives is required. Second, the course between the Scylla of full holism and the Charybdis of structural-functional modularism must be plotted more distinctly. Third, methodologies better suited to reveal brain circuits must be brought in. Finally, the constraints that naturalistic settings provide should be considered.

Presenting evidence from the social brain, we argue that neural reuse is a dynamic, socially organized process that is influenced ontogenetically and evolutionarily by the cultural transmission of mental techniques, values, and modes of thought. Anderson's theory should be broadened to accommodate cultural effects on the functioning of architecturally similar neural systems, and the implications of these differences for reuse.

Novel functions, which emerge by reusing existing resources formerly adapted to other original usages, cannot be anticipated before the need eventually arises. Simple reuse must be accidental. However, to survive the evolutionary race, one cannot merely keep hoping for a string of good fortune. So, successful species might be gifted with “rational” and “purposeful” biological mechanisms to prepare for future reuse. Neural reuse must be extrapolated from such mechanisms.

Anderson's theory is plausible and largely consistent with the data. However, it remains underspecified on several fronts, and we highlight areas for potential improvement. Reuse is described as duplicating a functional component, preserving one function and tinkering to add another function. This is a promising model, but Anderson neglects other reasonable alternatives and we highlight several. Evidence cited in support of reuse fails to uniquely support it among a broader set of multi-use theories. We suggest that a more stringent criterion for direct support of reuse may be satisfied by focusing on previous adaptive functions (original use).

Comparative studies demonstrate that homologous neural structures differ in function and that neural mechanisms underlying behavior evolved independently. A neural structure does not serve a particular function so much as it executes an algorithm on its inputs though its dynamics. Neural dynamics are altered by a neuromodulation, and species-differences in neuromodulation can account for behavioral differences.

Anderson's massive redeployment hypothesis (MRH) takes the grounding of meaning in sensorimotor behaviour to be a side effect of neural reuse. I suggest this grounding may play a much more fundamental role in accounting for the bootstrapping of higher-level cognition from sensorimotor behaviour. Thus, the question of when neural reuse delivers semantic inheritance is a pressing one for MRH.

Anderson's meta-analysis of fMRI data is subject to a potential confound. Areas identified as active may make no functional contribution to the task being studied, or may indicate regions involved in the coordination of functional networks rather than information processing per se. I suggest a way in which fMRI adaptation studies might provide a useful test between these alternatives.

This commentary suggests how the target article raises new implications for brain injury therapies, which may have been anticipated by the neurologist Kurt Goldstein, though he worked in and earlier era of fervent localization of brain function.

Chemistry, genetics, physics, and linguistics all present instances of reuse. I use the example of how behavioral constraints may have contributed to the emergence of phonemic reuse. Arising from specific facts about speech production, perception, and learning, such constraints suggest that combinatorial reuse is domain-specific. This implies that it would be more prudent to view instances of neural reuse not as reflecting a “fundamental organizational principle,” but as a fortuitous set of converging phenomena.

With his massive redeployment hypothesis (MRH), Anderson claims that novel cognitive functions are likely to rely on pre-existing circuits already possessing suitable resources. Here, we put forward recent findings from studies in numerical cognition in order to show that the role of sensorimotor experience in the ontogenetical development of a new function has been largely underestimated in Anderson's proposal.