Uniquely human developmental timing may drive cerebral lateralization and interhemispheric coupling

Uniquely human developmental timing may drive cerebral lateralization and interhemispheric collaboration Ben Cipollini (bcipolli@cogsci.ucsd.edu) Department of Cognitive Science, 9500 Gilman Dr La Jolla, CA 92093 USA Garrison Cottrell (cottrell@eng.ucsd.edu) Department of Computer Science and Engineering, 9500 Gilman Dr La Jolla, CA 92093 USA Abstract brains. Whether or not the delay magnitude hypothesis is cor- rect, it certainly is not complete. We hypothesize that functional lateralization is not caused by the magnitude of conduction delays. First, we’ll review literature that supports our hypothesis. We’ll present a re- analysis of Ringo et al. (1994) that severely restricts the scope of their results. We’ll propose a new hypothesis that the de- velopmental trajectory of human brains enables functional lateralization–specifically, that the vast and accelerated post- natal expansion of brain size and delayed maturation of the corpus callosum causes unreliable timing of interhemispheric information in pre-adult humans. We’ll review literature sup- porting this hypothesis, then we’ll present our own model supporting the plausibility of our developmentalhypothesis. Finally, we’ll summarize our results and discuss implications of our findings to the general phenomena of lateralization, asymmetry, and cognition. Cerebral lateralization is intertwined with virtually every cog- nitive function that we think makes us human. Yet a clear di- chotomy has never been explained: lateralized processing sug- gests independent, local development of neural circuits, but the complementary nature of lateralized functions and extremely strong functional coupling between homologous areas suggest robust interhemispheric interactions. Here, we review litera- ture and present modeling evidence that this dichotomy can be explained by the uniquely steep trajectory of human post-natal brain growth. This drastic volumetric change cause most long distance, interhemispheric connections to be more unreliable than shorter, intrahemispheric connections, leading to lateral- ization. Strong interhemispheric collaboration is enabled by the later maturation and myelination of long-distance callosal connections. We also review and reanalyze a well-cited model- ing paper (Ringo, Doty, Demeter, and Simard (1994)) thought to show a relationship between the degree of hemispheric co- ordination and length of conduction delays, showing that pre- vious claims have a clear alternative explanation. Keywords: corpus callosum; lateralization; asymmetry; con- duction delays; The failure of conduction delay magnitude Callosal axons are especially long in humans, due to their need to traverse through our large, highly gyrified brains to connect to the opposite hemisphere. Because the average con- duction velocity of axons does not sufficiently compensate for the additional axon lengths when compared to smaller- brained animals, the resulting interhemispheric transmission delay over the majority of callosal axons is longer in human brains. The delay magnitude hypothesis suggests that this increased delay would cause less interhemispheric collabora- tion and therefore enable cerebral asymmetry. While the anatomy and physiology of callosal axons is well-established, their seemingly intuitive effects on inter- hemispheric collaboration is supported by a single model in a single paper (Ringo et al., 1994). Here, we argue against the delay magnitude hypothesis in two parts. First, we present 4 results from the literature that are inconsistent with the delay magnitude hypothesis. Second, we show that the model itself does not support the hypothesis. Introduction A single concept, supported by a single paper, has dominated thought as to the origins of cerebral lateralization. The mod- eling work of Ringo et al. (1994) has been exclusively and extensively cited to support the notion that large magnitude conduction delays, due to the large human brain size, enable cerebral lateralization. This delay magnitude hypothesis has intuitive appeal, as it supports another long-held notion: that some combination of large brains and functional lateraliza- tion have made us human. There is no denying the importance of functional later- alization in human cognitive abilities; we are functionally lateralized in virtually all cognitive functions that we think are special to our species, including language, high-precision manual use of tools, spatial processing abilities, and even our emotional processing (Gazzaniga, 2000; Craig, 2005). There is also no denying, however, that the lateralized hemispheres are also tightly coupled in terms of both their complemen- tary abilities (Gazzaniga, 2000; Hellige, 2006) and their func- tional coupling (Stark et al., 2008). This dichotomy is simply not captured by the delay magnitude hypothesis. Nor does the hypothesis account for the anatomical and functional asym- metries that appear throughout the animal kingdom (Rogers & Andrew, 2002; Rogers, 2009) in organisms with small 1. Increased interhemispheric collaboration is associated with an increase in slow fibers Larger corpus callosum size is associated with less lateral- ization. This is true for regions of the corpus callosum, as well as the corpus callosum as a whole. The midbody of the callosum, which carries fibers to and from motor