Nature, nurture and some randomness

Since Sir Francis Galton famously framed the “nature vs. nurture” debate in 1869, most scientists have thought that it is a combination of genetics (nature) and sensory experience (nurture) that guides how the brain wires to result in different behavioral outputs. The notion that nature and nurture might work together comes from studies done on monozygotic twins (almost identical genetic material) who were brought up separately often display more similar behavioral traits than dizygotic twins or siblings. The higher behavioral similarity would suggest that nature plays a role. However, the fact that there still are some behavioral differences remains at present the best evidence that nurture is important as well. Interestingly, a recent meta-analysis study published in Nature Genetics that looks at all twin studies performed in the past 50 years argues that the contributions of nature and nurture on behavior are pretty much 50-50 (Polderman et al. 2015).

Taking these ideas to a more synaptic level, a large number of studies have identified a variety of molecules involved in the development of neuronal connections that function either in an activity-independent manner (nature) or in response to neuronal activity likely in the form of sensory stimulation (nurture). However, are these activity-independent molecules and neuronal activity the only two contributors to brain wiring? Could we imagine a scenario where both these factors are equal and yet only one connection has to be chosen? How would this occur? Could there be other factors perhaps like randomness?

In Neuron this past month, Owens et al. (2015) show evidence for randomness in the form of stochastic interaction between the activity-independent molecules and activity-dependent mechanisms of topographic map formation in the superior colliculus (the first brain area that neurons from the retina connect to). It has already been demonstrated that the projections from the retina to the superior colliculus are sculpted by both molecular cues (Ephrin and EphA receptor gradients) as well as neuronal activity (spontaneous activity waves). In mice where either ephrin signaling or spontaneous activity is blocked, the topographic map is disrupted. However, this strategy cannot tell us how the two factors interact to produce the final topographic map. In this paper, the authors use intrinsic signal optical imaging in transgenic mice where both ephrin signaling and activity are present but no longer acting in concert to investigate the relationship between molecular cues and activity. The authors demonstrate that there is a high level of heterogeneity in the organization of retinocollicular inputs in these mice that is best explained by a stochastic model where some connections are organized by molecular cues while some are organized by activity in a random manner.

While it is inevitable that there is some degree of randomness and noise in the nervous system, it is commonly believed that the nervous system works towards minimizing this randomness. Contrarily, the Owens et al. paper demonstrates a role for randomness in nervous system development. These results make me wonder what other processes may be driven in a stochastic manner and why this may be beneficial to us. A stochastic system might promote faster topographic establishment or perhaps allow for greater variation and adaptability. Nevertheless, it is interesting to think that perhaps our brain is nature, nurture and a little bit of random.

Reference:

  • Owens, M.T., Feldheim, D.A., Stryker, M.P., Triplett, J.W. (2015) Stochastic interaction between neural activity and molecular cues in the formation of topographic maps Neuron 87, 1261-1273
  • Polderman, T.J.C., Benyamin, B., de Leeum, C.A., Sullivan, P.F., van Bochoven, A. Visscher, P.M., Posthuman, D. (2015) Meta-analysis of the heritability of human traits based on fifty years of twin studies Nature Genetics Vol. 47 No. 7
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  1. Nature, nurture and a little bit of random… Maybe part of that ‘little bit of random’ lies in the proces of acquired somatic mutations in neurons as shown by Lodato MA et al in http://m.sciencemag.org/content/350/6256/94.abstract. Interestingly enough mutations seem to be down to gene transcription. So, nature or nurture?

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