March 23, 2012

Use, Reuse, and Use Again.....

One commonly assumed feature of the brain is that widespread plasticity is responsible for behavioral variation. While this has indeed been demonstrated for cortical regions of mammals [1,2], by and large its relationship to evolutionary processes is unclear. Related to this are the origins of cultural behaviors in humans. While cultural behaviors are not limited to humans, the scope of human dependence on culture is unique. Therefore, an important issue in the brain sciences is how cultural behaviors are represented in the brain. This involves both the origin of neuronal circuits and changes in these circuits across species.

Is this due to plasticity or some other mechanism? Some specialization of the neuronal architecture is likely required in order to enable specific cultural behaviors and subsequent cultural evolution within a species. But does this proceed in a way analogous to massive cortical plasticity, or does it build upon previously defined circuits? There are a variety of views on this in the literature, but the consensus seems to be that an evolutionary mechanism called exaptation is primarily responsible for the origins question. Exaptation is the functional redeployment of a trait that originally evolved for another purpose. In [3], the author uses the term reuse to characterize the redeployment of conserved neural circuits for cultural behaviors in humans. There are several competing theories that fall under this category, but the neuronal recycling [4] and massive redeployment [5] models suggest that these changes are related to development and evolution, respectively.

Figure 1. Comparision of anatomical modularity (TOP) with reuse (BOTTOM) as the driver of functional changes in a six-region representation of the brain. Solid and dashed lines represent two different cognitive functions. COURTESY: Figure 1 from [3].

Focusing on evolutionary origins, there are several predictions made in the massive redeployment model. One of these is that when a new function arises (such as mathematical reasoning or reading), incorporation of these functions into existing circuits should be favored over the formation of new circuits. Accordingly, there should be a correlation between the phylogenetic ancient-ness of a brain area and it's frequency of reuse. Finally, more recently derived functions should use a greater number of circuits which are more widespread in the brain. Evidence for these ideas can be seen in a meta-analysis of fMRI data [6]. Using a subtraction approach and accounting for 11 task domains, a typical cortical region is activated by up to nine of these domains [6].

Dehaene and Cohen more explicitly connect the neuronal recycling model to the origins of culture in [7]. According to their work, representations of letter and number sequences can be localized to the left occipital and bilateral intraparietal areas of the brain (see Figure 2). Importantly, these areas have two attributes that is important for redeploying existing brain areas for cultural behavior. One of these is a systematic architecture that allows for complex representations. The other involves repeatable activation patterns (as revealed by neuroimaging). The importance of repeatable activation related to other functions can be appreciated when considering cultural symbols that are invariant (e.g. a universal response) in a cross-cultural context and having their origins in non-cultural stimuli [see 8 for more information].

Figure 2. Locations for activation in the left occipital and bilateral intraparietal cortices involving both newer (letter and number processing) and older (non-word stimuli) functions for these areas. COURTESY: Figure 1 from [7].

In [7], the authors hypothesize that neuronal recycling is related to behaviors and neuronal processing observed among cultural traits (e.g. writing and numeracy) in three ways. The first is that although phylogenetically-old areas can indeed be redeployed, they are also constrained in evolution and development. Developmental constraints are particularly important in that they bias acquisition and learning during life-history. The second relation involves the existence of a neuronal niche for cultural acquisitions. It does not appear that exaptation proceeds randomly. Instead, areas that already serve a related function are more likely to be repurposed for newer functions. In the case of regions proposed by Dehaene and Cohen, previous functions related to scene and object recognition are well-suited to recognition of cultural symbols. Because of this, these previous organizational attributes are not erased upon repurposing, thus enabling future repurposing.

To understand the phenomenon of neural reuse and evolutionary relationships in another light, I will turn to a recent article in Nature Methods [9] that describes how we can determine functional equivalence across species with respect to functional evolutionary changes. If the exaptation of phylogenetically-conserved regions drives the neural representation of new behaviors, then understanding commonalities of neural representation across species is important. Here I make the distinction between "functional equivalence" and homology in part because previous research [10] has shown that neural homology (based on structure) is exceedingly hard to establish. Unlike many other morphological traits, neural traits often change position and recombine, which makes establishing their common ancestry difficult.

To assess common processing for natural scenes between monkeys (Macaca mulatta) and humans, a method called interspecies activity correlation (ISAC) was used to determine functionally-equivalent regions.Figure 3 graphically demonstrates the ISAC method in stepwise fashion.

Figure 3. Diagram of the ISAC method as applied to monkey and human brains. ROI = region of interest. COURTESY: Figure 1 from [9].

ISAC does not rely on the inference of anatomical relationships. Instead, ISAC is a statistical technique that equates correlated brain region-specific hemodynamic activity with commonalities activation patterns between species. When a common stimulus is presented (in this case natural scenes), a time-course of neural activity is collected for each species. Using both correlational and convolutional analysis techniques, species-specific hemodynamic signals can then be compared on a voxel by voxel basis. In the future, this might be one way to assess systematic architectures and repeatable activation patterns.

So are brain regions used, reused, and used again for new functions that emerge in the course of evolution? There seems to be a lot of interesting work that points in this direction. The evolutionary concept of exaptation [11] provides a mechanism for this continued reuse across phylogeny, while cutting-edge neuroimaging techniques provide a window (albeit opaquely) into this evolutionary relationship. By identifying both the conserved and derived functions of different brain regions, we might be able to fill in the boxes shown in Figure 1 with specific examples of exaptation in the brain for evolutionarily-derived cognitive functions.


[1] Krubitzer, L. and Kahn, D. (2003). Nature versus nurture revisited: an old idea with a new twist. Progress in Neurobiology, 70(1), 33-52.

[2] Kaas, J. and Catania, K. (2002). How do features of sensory representations develop? BioEssays, 24, 334-343.

[3] Anderson, M.L. (2010). Neural reuse: A fundamental organizational principle of the brain. Behavioral and Brain Sciences, 33, 245–313.

[4] Dehaene, S. and Cohen, L. (2007). Cultural recycling of cortical maps. Neuron, 56, 384–398.

[5] Anderson, J.R. (2007). How can the human mind occur in the physical universe? Oxford University Press, Oxford, UK.

[6] Anderson, M.L. (2007). Evolution of cognitive function via redeployment of brain areas. The Neuroscientist 13, 13–21.

[7] Dehaene, S. and Cohen, L. (2007). Cultural Recycling of Cortical Maps. Neuron, 56, 384-398.

[8] Changizi, M.A., Zhang, Q., Ye, H., and Shimojo, S. (2006). The structures of letters and symbols throughout human history are selected to match those found in objects in natural scenes. American Naturalist, 167, E117–E139.

[9] Mantini, D. (2012). Interspecies activity correlations reveal functional correspondence between monkey and human brain areas. Nature Methods, 9(3), 277-282. For more on using neuroimaging to establish "homology", please see: Wager, T.D. and Yarkoni, T. (2012). Establishing homology between monkey and human brains. Nature Methods, 9(3), 237-239.

[10] Striedter, G.F. (2002). Brain homology and function: an uneasy alliance. Brain Research Bulletin, 57, 239–242. AND Sereno, M.I. and Tootell, R.B.H. (2005). From monkeys to humans: what do we now know about brain homologies? Current Opinion in Neurobiology, 15, 135–144.

[11] Okada, N., Sasaki, T., Shimogori, T., and Nishihara, H. (2010). Emergence of mammals by emergency: exaptation. Genes to Cells, 15(8), 801-812.

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