Clonally Related Visual Cortical Neurons Show Similar Stimulus Feature Selectivity

Division of Neurobiology, Department of Molecular and Cell Biology, University of California, Berkeley, California 94720, USA.
Nature (Impact Factor: 41.46). 06/2012; 486(7401):118-21. DOI: 10.1038/nature11110
Source: PubMed


A fundamental feature of the mammalian neocortex is its columnar organization. In the visual cortex, functional columns consisting of neurons with similar orientation preferences have been characterized extensively, but how these columns are constructed during development remains unclear. The radial unit hypothesis posits that the ontogenetic columns formed by clonally related neurons migrating along the same radial glial fibre during corticogenesis provide the basis for functional columns in adult neocortex. However, a direct correspondence between the ontogenetic and functional columns has not been demonstrated. Here we show that, despite the lack of a discernible orientation map in mouse visual cortex, sister neurons in the same radial clone exhibit similar orientation preferences. Using a retroviral vector encoding green fluorescent protein to label radial clones of excitatory neurons, and in vivo two-photon calcium imaging to measure neuronal response properties, we found that sister neurons preferred similar orientations whereas nearby non-sister neurons showed no such relationship. Interestingly, disruption of gap junction coupling by viral expression of a dominant-negative mutant of Cx26 (also known as Gjb2) or by daily administration of a gap junction blocker, carbenoxolone, during the first postnatal week greatly diminished the functional similarity between sister neurons, suggesting that the maturation of ontogenetic into functional columns requires intercellular communication through gap junctions. Together with the recent finding of preferential excitatory connections among sister neurons, our results support the radial unit hypothesis and unify the ontogenetic and functional columns in the visual cortex.

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Article: Clonally Related Visual Cortical Neurons Show Similar Stimulus Feature Selectivity

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    • "There has been significant interest in the role that clonal relationships might play in the organization of cortical neurons. It has been previously suggested that clonal identity could influence the connectivity of sibling cells within cortical circuits (Li et al., 2012; Sultan et al., 2014; Yu et al., 2012). The clustered appearance of radially and horizontally aligned interneurons following sparse viral labeling is visually striking and appears to support the idea that clonal relationships dictate these alignments (Brown et al., 2011; Ciceri et al., 2013). "
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    • "In the developing neocortex of very young mice, it was reported that inhibitory interneurons originating from the same progenitor cells were distributed in a clustered manner, although visual responsiveness of these interneurons was not studied (Brown et al., 2011; Ciceri et al., 2013). It seems possible that those interneurons might form functional clusters of neurons with similar responsiveness after eye opening, because ''sister'' neurons in the same radial clone exhibit similar orientation preferences (Li et al., 2012; Ohtsuki et al., 2012). However, the previous findings were obtained from excitatory or unclassified neurons, and thus a question of whether inhibitory interneurons derived from the same progenitor cells have similar visual response properties is still open to be addressed in future studies. "
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