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: 42.35). 06/2012; 486(7401):118-21. DOI: 10.1038/nature11110
Source: PubMed

ABSTRACT 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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Available from: Hua-tai Xu, Dec 31, 2013
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    • "Since then, the use of Cre-loxP technology has been widely extended in the scientific community by combining it with fluorescent reporter genes, increasing dramatically the possibilities to study cell lineages and/or mapping neural circuits, as reported by Brainbow technology (Livet et al., 2007; Cai et al., 2013). Another approach is using modified retrovirus to label cell lineages by infecting progenitors (Cepko et al., 1995; Reid et al., 1995; Li et al., 2012), a widely used technology for tracking cells (Heins et al., 2002; Weber et al., 2011). The use of virus with the purpose of tracking cells or modifying their phenotypes is a widely used technology (Heins et al., 2002; Weber et al., 2011). "
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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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    • "peaking at, the location of the corresponding barrel in the barrel field, indicating that neurons sharing similar receptive field properties are also grouped into barrel-related columns in the somatosensory cortex of the reeler mouse and demonstrating that information flow into the cortex retains a columnar organizing principle in the otherwise disorganized reeler cortex (Mountcastle et al. 1955; Mountcastle 1957, 1997; Petersen and Sakmann 2001; Horton and Adams 2005; Feldmeyer et al. 2013). During cortical development, newly generated neurons deriving from common progenitors migrate radially into the cortex where they form networks of sibling neurons sharing similar receptive field properties, and the reeler functional columnar modules revealed by the present study are therefore likely to be composed of neurons sharing a common lineage (Rakic 1988; Yu et al. 2012; Li et al. 2012). Together with the correct positioning of the somatosensory cortex within the cortical mantle, this observation can be reconciled with the view that cortical development involves the projection of an arealized protomap already existing at the level of the early proliferative cortical sheet onto the developing cortical plate through the radial migration of newborn neurons, since only the radial, and not tangential, organization of the barrel field is compromised in reeler (Rakic 1988). "
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