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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Available from: Hua-tai Xu, Dec 31, 2013
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    • "Visual stimuli recruit intrinsically generated cortical circuits of neurons (ensembles) during embryogenesis prior to visual experience as a result of spontaneous activity generated in the retina (Shatz, 1996; retinal and cortical waves). An alternative proposed process involves gap junctions coupling of clonally related neurons at prenatal developmental stage (Li et al., 2012). In both cases, FIGURE 1 | Schematic model of the innate control of adaptive memory strategies in the immune system (IS) and central nervous system (CNS). "
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    • "Visual stimuli recruit intrinsically generated cortical circuits of neurons 401 (ensembles) during embryogenesis prior to visual experience as a result of spontaneous 402 activity generated in the retina (Shatz 1996) (retinal and cortical waves). An alternative 403 proposed process involves gap junctions coupling of clonally related neurons at prenatal 404 developmental stage (Li, Lu et al. 2012). In both cases, a selective competitive process 405 requiring the formation and elimination of synaptic connections takes place (Shatz 406 1996). "
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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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