Sensory maps in the olfactory cortex defined by long-range viral tracing of single neurons

Department of Cell Biology, Dorris Neuroscience Center, The Scripps Research Institute, La Jolla, California 92037, USA.
Nature (Impact Factor: 41.46). 03/2011; 472(7342):217-20. DOI: 10.1038/nature09945
Source: PubMed


Sensory information may be represented in the brain by stereotyped mapping of axonal inputs or by patterning that varies between individuals. In olfaction, a stereotyped map is evident in the first sensory processing centre, the olfactory bulb (OB), where different odours elicit activity in unique combinatorial patterns of spatially invariant glomeruli. Activation of each glomerulus is relayed to higher cortical processing centres by a set of ∼20-50 'homotypic' mitral and tufted (MT) neurons. In the cortex, target neurons integrate information from multiple glomeruli to detect distinct features of chemically diverse odours. How this is accomplished remains unclear, perhaps because the cortical mapping of glomerular information by individual MT neurons has not been described. Here we use new viral tracing and three-dimensional brain reconstruction methods to compare the cortical projections of defined sets of MT neurons. We show that the gross-scale organization of the OB is preserved in the patterns of axonal projections to one processing centre yet reordered in another, suggesting that distinct coding strategies may operate in different targets. However, at the level of individual neurons neither glomerular order nor stereotypy is preserved in either region. Rather, homotypic MT neurons from the same glomerulus innervate broad regions that differ between individuals. Strikingly, even in the same animal, MT neurons exhibit extensive diversity in wiring; axons of homotypic MT pairs diverge from each other, emit primary branches at distinct locations and 70-90% of branches of homotypic and heterotypic pairs are non-overlapping. This pronounced reorganization of sensory maps in the cortex offers an anatomic substrate for expanded combinatorial integration of information from spatially distinct glomeruli and predicts an unanticipated role for diversification of otherwise similar output neurons.

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    • "The finding that the male and female stimuli activate different parts of the PIR and ENT areas suggests that topologically distinct MOB cortical outputs may discriminate the sexspecific stimuli. This dorsoventral separation is an example of a novel spatial organization in the piriform cortex, which until now has been considered to lack gross sensory input-based topology (Ghosh et al., 2011; Sosulski et al., 2011). "
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    ABSTRACT: Central to the understanding of brain functions is insight into the distribution of neuronal activity that drives behavior. Local measurements of brain activity in behaving mice can be made with electrodes and fluorescent calcium indicators (Buzsáki, 2004 and Grewe and Helmchen, 2009), but such approaches provide information regarding only a very small fraction of the ∼70 million neurons that comprise the mouse brain. The detection of elevated levels of the immediate-early genes (IEGs) linked to recent neuronal activity (Clayton, 2000 and Guzowski et al., 2005) is a more spatially comprehensive technique. While it lacks the time resolution of electrophysiological recordings or calcium imaging, it does have the potential of providing a complete view of recent whole-brain activity. Once determined, the whole-brain IEG-based map can be used to generate structure-function hypotheses to be probed by high-resolution recordings as well as optogenetic and chemogenetic methods (Fenno et al., 2011 and Lee et al., 2014).
    Cell Reports 12/2014; 71(2). DOI:10.1016/j.celrep.2014.12.014 · 8.36 Impact Factor
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    • "There is evidence that some of the OT does not reach the bulbs directly via these neural projections (Yu et al., 1996a; Yu et al., 1996b), and transport of OT via the cerebrospinal fluid is possibly one of the mechanisms involved (Veening et al., 2010; Veening and Olivier, 2013). OT can directly affect neuronal processing in the bulb itself and in addition many amygdaloid and other limbic brain areas contain OT-receptors (Ghosh et al., 2011; Gimpl and Fahrenholz, 2001; Kang et al., 2009; 2011; Miyamichi et al., 2011; Nagayama et al., 2010; Sosulski et al., 2011) and may be influenced by a local release of OT. Similar mechanisms have been studied extensively in sheep (Kendrick, 2000; Kendrick et al., 1997; Kendrick et al., 1986; Kendrick et al., 1991). "
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    ABSTRACT: Oxytocin (OT) is a nonapeptide with an impressive variety of physiological functions. Among them, the 'prosocial' effects have been discussed in several recent reviews, but the direct effects on male and female sexual behavior did receive much less attention so far. As our contribution to honor the lifelong interest of Berend Olivier in the control mechanisms of sexual behavior, we decided to explore the role of OT in the present review. In the successive sections, some physiological mechanisms and the 'pair-bonding' effects of OT will be discussed, followed by sections about desire, female appetitive and copulatory behavior, including lordosis and orgasm. At the male side, the effects on erection and ejaculation are reviewed, followed by a section about 'premature ejaculation' and a possible role of OT in its treatment. In addition to OT, serotonin receives some attention as one of the main mechanisms controlling the effects of OT. In the succeeding sections, the importance of OT for 'the fruits of labor' is discussed, as it plays an important role in both maternal and paternal behavior. Finally, we pay attention to an intriguing brain area, the ventrolateral part of the ventromedial hypothalamic nucleus (VMHvl), apparently functioning in both sexual and aggressive behavior, which are at first view completely opposite behavioral systems.
    European Journal of Pharmacology 07/2014; 753. DOI:10.1016/j.ejphar.2014.07.045 · 2.53 Impact Factor
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    • "This anatomical organization may underlie the fact that mitral and tufted cells project to the OC through different pathways and toward different targets suggesting the possibility that they carry different odor information (reviewed in Mori and Sakano, 2011). The diverse cortical projections of a single mitral cell, the broad distribution of mitral cells axons and the overlapping of their information at their target neurons provide the basis for a diversification and combinatorial integration of the olfactory information processing (Ghosh et al., 2011). Recent work using anatomical and physiological techniques demonstrated that individual neurons in the piriform cortex receive convergent input from mitral/tufted cells connected to multiple glomeruli located all over the OB (Apicella et al., 2010; Davison and Ehlers, 2011; Miyamichi et al., 2011). "
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    ABSTRACT: authors have contributed equally to this work. The olfactory system has a highly regular organization of interconnected synaptic circuits from the periphery. It is therefore an excellent model for understanding general principles about how the brain processes information. Cajal revealed the basic cell types and their interconnections at the end of the XIX century. Since his original descriptions, the observation and analysis of the olfactory system and its components represents a major topic in neuroscience studies, providing important insights into the neural mechanisms. In this review, we will highlight the importance of Cajal contributions and his legacy to the actual knowledge of the olfactory system.
    Frontiers in Neuroanatomy 07/2014; 8. DOI:10.3389/fnana.2014.00055 · 3.54 Impact Factor
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