Non-redundant odor coding by sister mitral cells revealed by light addressable glomeruli in the mouse

Dhawale, Ashesh K.; Hagiwara, Akari; Bhalla, Upinder S.; Murthy, Venkatesh N.; Albeanu, Dinu F.

doi:10.1038/nn.2673

Cited by 220 publications

(270 citation statements)

References 49 publications

(59 reference statements)

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“…Because our focus was to study the functional role of MC intrinsic diversity, we chose not to include any of the effects of neural connections such as synapses between neurons in our experiments and simulations. Given that the olfactory bulb possesses extensive lateral circuitry (11), which has been shown to also diversify MC responses (11,39,40), we expect that bulbar circuit activity will work in conjunction with intrinsic diversity in vivo to further diversify MC responses (41). Furthermore, when decoding we took the perspective that the best populations were those that resulted in the most faithful reconstruction of the stimulus.…”

Section: Discussionmentioning

confidence: 99%

Intermediate intrinsic diversity enhances neural population coding

Tripathy

Padmanabhan

Gerkin

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

128

125

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Cell-to-cell variability in molecular, genetic, and physiological features is increasingly recognized as a critical feature of complex biological systems, including the brain. Although such variability has potential advantages in robustness and reliability, how and why biological circuits assemble heterogeneous cells into functional groups is poorly understood. Here, we develop analytic approaches toward answering how neuron-level variation in intrinsic biophysical properties of olfactory bulb mitral cells influences population coding of fluctuating stimuli. We capture the intrinsic diversity of recorded populations of neurons through a statistical approach based on generalized linear models. These models are flexible enough to predict the diverse responses of individual neurons yet provide a common reference frame for comparing one neuron to the next. We then use Bayesian stimulus decoding to ask how effectively different populations of mitral cells, varying in their diversity, encode a common stimulus. We show that a key advantage provided by physiological levels of intrinsic diversity is more efficient and more robust encoding of stimuli by the population as a whole. However, we find that the populations that best encode stimulus features are not simply the most heterogeneous, but those that balance diversity with the benefits of neural similarity.generalized linear models | intrinsic biophysics | neural variability | stimulus coding | ion channels B iological systems including brains must function efficiently under many constraints, including constraints on the numbers of individual neurons dedicated to a given task. Brain function therefore depends on an appropriate division of labor, with specific neurons dedicated to different functions. For example, different types of retinal ganglion cells represent visual information at different timescales (1), and distinct classes of cortical interneurons play diverse roles in coordinating network activity (2). Whereas attempts to understand how distinct classes of cells encode information have proven successful (1), the importance of within-type variability remains poorly understood (3, 4) although has recently become a topic of great interest (5-8).Although neuron-to-neuron variability is often viewed as an epiphenomenon of biological imprecision (3, 4), having neurons of the same type that respond to different stimulus features may improve stimulus encoding. This variability may be leveraged to improve functions such as stimulus encoding if heterogeneous output of neurons of a single type is collectively used for population coding. Such populations of neurons could efficiently represent complex stimuli by collectively covering the relevant stimulus space (1, 9, 10). Network interactions could further increase the efficiency of information transmission by decorrelating neural responses and reducing the redundancy between their outputs (11-13). In contrast, eliminating redundancy (also referred to as biological degeneracy, ref. 14) may make stimulus coding less robu...

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Section: Discussionmentioning

confidence: 99%

Intermediate intrinsic diversity enhances neural population coding

Tripathy

Padmanabhan

Gerkin

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

128

125

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“…Indeed, there is evidence of such an increased dynamic range in Drosophila, where glomerular projection neurons (similar to mitral cells) fire with more sensitivity and reliability in response to a wider range of odorants than the olfactory receptor neurons that feed into them (Bhandawat et al 2007). Additionally, a recent study in mice demonstrates that the spike timing of the mitral/tufted cells innervating the same glomerulus is differentially altered by odor stimulation (Dhawale et al 2010). Further studies are required to understand how the olfactory system processes the temporally distinct firing patterns carried by OSNs expressing the same receptor.…”

Section: Discussionmentioning

confidence: 99%

Spontaneous and sensory-evoked activity in mouse olfactory sensory neurons with defined odorant receptors

Connelly

Savigner

2013

Journal of Neurophysiology

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Connelly T, Savigner A, Ma M. Spontaneous and sensory-evoked activity in mouse olfactory sensory neurons with defined odorant receptors. J Neurophysiol 110: 55-62, 2013. First published April 17, 2013 doi:10.1152/jn.00910.2012.-Sensory systems need to tease out stimulation-evoked activity against a noisy background. In the olfactory system, the odor response profile of an olfactory sensory neuron (OSN) is dependent on the type of odorant receptor it expresses. OSNs also exhibit spontaneous activity, which plays a role in establishing proper synaptic connections and may also increase the sensitivity of the cells. However, where the spontaneous activity originates and whether it informs sensory-evoked activity remain unclear. We addressed these questions by examining patch-clamp recordings of genetically labeled mouse OSNs with defined odorant receptors in intact olfactory epithelia. We show that OSNs expressing different odorant receptors had significantly different rates of basal activity. Additionally, OSNs expressing an inactive mutant I7 receptor completely lacked spontaneous activity, despite being able to fire action potentials in response to current injection. This finding strongly suggests that the spontaneous firing of an OSN originates from the spontaneous activation of its G protein-coupled odorant receptor. Moreover, OSNs expressing the same receptor displayed considerable variation in their spontaneous activity, and the variation was broadened upon odor stimulation. Interestingly, there is no significant correlation between the spontaneous and sensory-evoked activity in these neurons. This study reveals that the odorant receptor type determines the spontaneous firing rate of OSNs, but the basal activity does not correlate with the activity induced by near-saturated odor stimulation. The implications of these findings on olfactory information processing are discussed.

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“…Odour acquisition can be tested by means of intermittent testing with odorant pairs which have already been acquired. (Modified from [3], Elsevier © 2004) ed specifically those mitral cells which receive input signals from the same glomerulus [17]. These"sister" mitral cells actually show very similar olfactory profiles to those expected on the basis of the genetic identity of the olfactory fibres converging in the glomerulus [18,19].…”

Section: Inhibitory Networkmentioning

confidence: 90%

Molecules, cells and networks involved in processing olfactory stimuli in the mouse olfactory bulb

Kuner

Schaefer

2011

E-Neuroforum

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How sensory stimuli are processed by neural networks is a key question of neuroscience. Olfactory conditioning experiments in mice demonstrated that odour processing is fast and stimulus-dependent. Selective genetic perturbation of the inhibitory circuitry in the first relay station of olfactory processing, the olfactory bulb, altered such discrimination times, with increased inhibition accelerating and decreased inhibition slowing down odour discrimination. This illustrates that inhibition fulfils a key role in sensory processing.

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Non-redundant odor coding by sister mitral cells revealed by light addressable glomeruli in the mouse

Cited by 220 publications

References 49 publications

Intermediate intrinsic diversity enhances neural population coding

Intermediate intrinsic diversity enhances neural population coding

Spontaneous and sensory-evoked activity in mouse olfactory sensory neurons with defined odorant receptors

Molecules, cells and networks involved in processing olfactory stimuli in the mouse olfactory bulb

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