Anderson thoroughly reviews neural reuse as a common brain mechanism for human cognitive functions to emerge. During evolution, whenever organisms were faced with a novel unforeseen environment, they had no other means to overcome any immediate problems than by reusing any materials at hand. So, neural reuse appears to be a truly “fundamental organization principle” (target article title). However, it remains an open question as to how human higher-cognitive functions appear as though they are “ensured” to “evolve” much quicker than via ordinary biological evolutionary processes (sect. 6.3, para. 1). To bridge this gap, I try to propose here a “more universal theory of neural reuse” (sect. 6.4, para. 5) grounded in a broader evolutionary framework.
Anderson's “massive redeployment hypothesis” (MRH) stands on two major observations – selectivity and localization are not central features of the brain (sect. 1, para. 1), and newer brain networks of cognitive functions tend to involve more brain areas than older ones (sect. 1.1, para. 1). Four other premises could be recognized further: (1) Biological systems are never ultimately efficient – systems require some redundancy to be stable, adaptable, and sustainable, leading extreme (over-adapted) efficiency to risk flexibility to survive novel situations. (2) A somewhat redundant brain structure would allow representational bistablility, for both the original and adapted functions. Such bistability, or “polysemy,” would support the use of metaphor in conceptual structure (sect. 4, para. 1). In addition, gains of further redundancy to stabilize this adapted alternative usage, perhaps by rapid brain expansion, would allow rapid construction of new neural-niche (sect. 4.6, para. 2). (3) Humans have attained unusually long post-reproductive life spans, particularly for females. Reuse-based acquisition of cognitive functions, and resulting accumulation of knowledge, continues over the whole lifespan, tending to peak in middle to old age. Hence, for semantic inheritance (sect. 7, para. 2) over generations to happen, some extra-genetic mechanisms are indispensable. Finally, (4) a “novel concept” (sect. 7, para. 1) that realizes neural reuse should not be found only in Homo sapiens, but precursors must exist in nonhuman primates (sect. 6.3, para. 3) and are perhaps also present in other extant taxa.
Evolution ushers diversity and complexity (or, adaptive radiation), perhaps through two major different paths: Species with short life spans and mass-reproduction adapt to environmental changes through variations in their numerous offspring, expecting at least a few to survive. Species with long life spans and low birth rates do so through an individual capacity to adapt. This is readily carried out through expansion of an organ to control adaptive behaviors – the primate brain, and that of humans in particular, is the extreme example. The latter evolutionary process may not be naïve mutation and selection, but rather like the Baldwin effect that initially induced modification, within the range of preprogrammed adaptation, stands by for later mutations to optimize it – modular structures and their exploratory behaviors are proposed to be essential to realize such a phenomenon (Kirshner & Gerhart 2005). The concept of reuse would reinforce this path. That is, slightly excessive redundancy of the brain, initially designed to stabilize a system against unexpected environmental noise, occasionally allowed the system to be polysemous. This newly acquired bistable state enabled systems to be reused for completely different functions in the future, maybe in combination with other parts of the brain. Such novel networks could wait for optimization through later genetic changes, perhaps induced by an emergent epigenetic factor, and become embedded in the environment as a result of the function of the network itself – thus, enabling post-reproductive inheritance. This hypothetical mechanism, referred to as “real-time neural niche-construction” (sect. 6.3, para. 4), seems to be supported by recently discovered concrete biological phenomena, which are described below.
Monkey intraparietal neurons normally coding body image could be trained to code a tool in a way equivalent with the hand holding it (sect. 6.3, para. 4; Iriki et al. Reference Iriki, Tanaka and Iwamura1996) – thus, bistable or polysemous for the hand or the tool. This functional plasticity might range within a fringe of the system prepared for body growth, which came across adaptable to “sudden elongation” by the tool. This accidentally established equivalence between body parts (hands) and tools, in turn demonstrated additional polysemic interpretations, that is, hands were extended towards tools (externalization of innate body), or alternatively, tools were assimilated into the body schema (internalization of external objects). This “self-objectification” process happened to adapt further for the mind and the intention to emerge (Iriki Reference Iriki2006). However, if this new function stays limited within existing neural machinery, it is merely plasticity, or a learning process. But the evidence suggests this is not the case – monkeys exhibited substantial expansion (detectable in each individual monkey) of the grey matter, including above cortical areas, during only a two-week tool-use training period (Quallo et al. Reference Quallo, Price, Ueno, Asamizuya, Cheng, Lemon and Iriki2009). This directly proves the phenomena previously suggested (and detected statistically in groups) that humans who are experts in certain cognitive domains tend to have slightly thicker grey matter in the part corresponding to the area subserving such mental functions. Concrete biological and genetic mechanisms realizing this expansion could be studied using the monkey paradigm in the near future.
Once a novel, alternative, bistable state was found to be useful, additional resources will be invested to stabilize the system, perhaps allowing further redundancy. Humans can induce such expansion intentionally, to create a better, more comfortable environmental niche. Subsequently, triggered by (extra-genetic, or epigenetic) factors embedded in such an environment, the corresponding neural niche in the brain could be reinforced further – thus, comprising recursive intentional niche construction (Iriki & Sakura Reference Iriki and Sakura2008). Indeed, human-specific cognitive characteristics (or polysemous bias) seem to be subserved mainly by these “expanded” brain areas (Ogagwa et al. 2010; in press). Some aspects of recently evolved cognitive functions resulting from such neural reuse could be the mind (as described above; Iriki Reference Iriki2006), language, or culture, all of which contribute remarkably to semantic inheritance of the benefits acquired during the unusually elongated human post-reproduction period. “Thus, the theory suggests a novel pathway by which Homo sapiens may have achieved its current high-level cognitive capacities” (target article, sect. 6.3, para. 4).
Anderson thoroughly reviews neural reuse as a common brain mechanism for human cognitive functions to emerge. During evolution, whenever organisms were faced with a novel unforeseen environment, they had no other means to overcome any immediate problems than by reusing any materials at hand. So, neural reuse appears to be a truly “fundamental organization principle” (target article title). However, it remains an open question as to how human higher-cognitive functions appear as though they are “ensured” to “evolve” much quicker than via ordinary biological evolutionary processes (sect. 6.3, para. 1). To bridge this gap, I try to propose here a “more universal theory of neural reuse” (sect. 6.4, para. 5) grounded in a broader evolutionary framework.
Anderson's “massive redeployment hypothesis” (MRH) stands on two major observations – selectivity and localization are not central features of the brain (sect. 1, para. 1), and newer brain networks of cognitive functions tend to involve more brain areas than older ones (sect. 1.1, para. 1). Four other premises could be recognized further: (1) Biological systems are never ultimately efficient – systems require some redundancy to be stable, adaptable, and sustainable, leading extreme (over-adapted) efficiency to risk flexibility to survive novel situations. (2) A somewhat redundant brain structure would allow representational bistablility, for both the original and adapted functions. Such bistability, or “polysemy,” would support the use of metaphor in conceptual structure (sect. 4, para. 1). In addition, gains of further redundancy to stabilize this adapted alternative usage, perhaps by rapid brain expansion, would allow rapid construction of new neural-niche (sect. 4.6, para. 2). (3) Humans have attained unusually long post-reproductive life spans, particularly for females. Reuse-based acquisition of cognitive functions, and resulting accumulation of knowledge, continues over the whole lifespan, tending to peak in middle to old age. Hence, for semantic inheritance (sect. 7, para. 2) over generations to happen, some extra-genetic mechanisms are indispensable. Finally, (4) a “novel concept” (sect. 7, para. 1) that realizes neural reuse should not be found only in Homo sapiens, but precursors must exist in nonhuman primates (sect. 6.3, para. 3) and are perhaps also present in other extant taxa.
Evolution ushers diversity and complexity (or, adaptive radiation), perhaps through two major different paths: Species with short life spans and mass-reproduction adapt to environmental changes through variations in their numerous offspring, expecting at least a few to survive. Species with long life spans and low birth rates do so through an individual capacity to adapt. This is readily carried out through expansion of an organ to control adaptive behaviors – the primate brain, and that of humans in particular, is the extreme example. The latter evolutionary process may not be naïve mutation and selection, but rather like the Baldwin effect that initially induced modification, within the range of preprogrammed adaptation, stands by for later mutations to optimize it – modular structures and their exploratory behaviors are proposed to be essential to realize such a phenomenon (Kirshner & Gerhart 2005). The concept of reuse would reinforce this path. That is, slightly excessive redundancy of the brain, initially designed to stabilize a system against unexpected environmental noise, occasionally allowed the system to be polysemous. This newly acquired bistable state enabled systems to be reused for completely different functions in the future, maybe in combination with other parts of the brain. Such novel networks could wait for optimization through later genetic changes, perhaps induced by an emergent epigenetic factor, and become embedded in the environment as a result of the function of the network itself – thus, enabling post-reproductive inheritance. This hypothetical mechanism, referred to as “real-time neural niche-construction” (sect. 6.3, para. 4), seems to be supported by recently discovered concrete biological phenomena, which are described below.
Monkey intraparietal neurons normally coding body image could be trained to code a tool in a way equivalent with the hand holding it (sect. 6.3, para. 4; Iriki et al. Reference Iriki, Tanaka and Iwamura1996) – thus, bistable or polysemous for the hand or the tool. This functional plasticity might range within a fringe of the system prepared for body growth, which came across adaptable to “sudden elongation” by the tool. This accidentally established equivalence between body parts (hands) and tools, in turn demonstrated additional polysemic interpretations, that is, hands were extended towards tools (externalization of innate body), or alternatively, tools were assimilated into the body schema (internalization of external objects). This “self-objectification” process happened to adapt further for the mind and the intention to emerge (Iriki Reference Iriki2006). However, if this new function stays limited within existing neural machinery, it is merely plasticity, or a learning process. But the evidence suggests this is not the case – monkeys exhibited substantial expansion (detectable in each individual monkey) of the grey matter, including above cortical areas, during only a two-week tool-use training period (Quallo et al. Reference Quallo, Price, Ueno, Asamizuya, Cheng, Lemon and Iriki2009). This directly proves the phenomena previously suggested (and detected statistically in groups) that humans who are experts in certain cognitive domains tend to have slightly thicker grey matter in the part corresponding to the area subserving such mental functions. Concrete biological and genetic mechanisms realizing this expansion could be studied using the monkey paradigm in the near future.
Once a novel, alternative, bistable state was found to be useful, additional resources will be invested to stabilize the system, perhaps allowing further redundancy. Humans can induce such expansion intentionally, to create a better, more comfortable environmental niche. Subsequently, triggered by (extra-genetic, or epigenetic) factors embedded in such an environment, the corresponding neural niche in the brain could be reinforced further – thus, comprising recursive intentional niche construction (Iriki & Sakura Reference Iriki and Sakura2008). Indeed, human-specific cognitive characteristics (or polysemous bias) seem to be subserved mainly by these “expanded” brain areas (Ogagwa et al. 2010; in press). Some aspects of recently evolved cognitive functions resulting from such neural reuse could be the mind (as described above; Iriki Reference Iriki2006), language, or culture, all of which contribute remarkably to semantic inheritance of the benefits acquired during the unusually elongated human post-reproduction period. “Thus, the theory suggests a novel pathway by which Homo sapiens may have achieved its current high-level cognitive capacities” (target article, sect. 6.3, para. 4).