Rats track odour trails accurately using a multi-layered strategy with near-optimal sampling

Khan, Adil G.; Sarangi, Manaswini; Bhalla, Upinder S.

doi:10.1038/ncomms1712

Cited by 103 publications

(148 citation statements)

References 35 publications

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“…S5). These stimuli were chosen to cover a wide range of input frequencies including the range of frequencies these neurons likely receive in vivo (29,31). We created homogeneous populations, each consisting of five copies of a single MC, and heterogeneous populations generated by randomly selecting five MCs from the recorded set with replacement.…”

Section: Intrinsic Diversity Enables Populations To Generalize Acrossmentioning

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: Intrinsic Diversity Enables Populations To Generalize Acrossmentioning

confidence: 99%

Intermediate intrinsic diversity enhances neural population coding

Tripathy

Padmanabhan

Gerkin

et al. 2013

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

128

125

View full text Add to dashboard Cite

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“…In principle, bilateral comparison of odor concentration provides instantaneous information about the odor gradient of the plume (Webster et al, 2001). Armed with this information the animal can track odors efficiently (Vickers, 2000;Willis and Avondet, 2005;Porter et al, 2006;Steck et al, 2010;Khan et al, 2012).…”

Section: Introductionmentioning

confidence: 99%

Laterality and Symmetry in Rat Olfactory Behavior and in Physiology of Olfactory Input

Parthasarathy

Bhalla

2013

J. Neurosci.

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Many species use bilateral sampling for odor-guided navigation. Bilateral localization strategies typically involve balanced and lateralized sensory input and early neuronal processing. For example, if gradient direction is estimated by differential sampling, then any asymmetry could bias the perceived direction. Subsequent neuronal processing can compensate for this asymmetry but requires the presence of mechanisms to track changes in asymmetry. A high degree of laterality is also important for differential sampling because spillover of signals will dilute the perceived odor gradient. In apparent contradiction to this model, both symmetry and laterality of nasal air flow have been reported to be incomplete in rats. Here, we measured symmetry and laterality in early olfactory processing in the rat. We first established behavioral readouts of precisely controlled bilateral odorant stimuli. We found that rats could rapidly and accurately report the direction of a wide range of odor gradients, presented in random sequence. We then showed that nasal air flow was symmetric over an entire day in awake rats. Furthermore, odor sampling from the two nostrils in the behavioral task was highly lateralized. This lateralization extended to the receptor epithelium responses as measured by electro-olfactograms. We finally observed strong lateralization of intrinsic signal responses from the glomerular layer of the olfactory bulb. We confirmed that a differential comparison of glomerular responses was sufficient to localize odorants. Together, these results suggest that the rat olfactory system is symmetric, with highly lateralized odor flow and neuronal responses. In combination, these attributes support odor localization by differential comparison.

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“…Male moths orient themselves towards conspecific females in response to sex pheromones by two patterns of locomotion: an initial surge and zig-zag casting behaviour [1][2][3] . Zig-zag locomotion has been reported in a wide range of animal species comprising of insects 4,5 and mammals 6 , including humans 7 . In moths, sex pheromones have been shown to reliably elicit stereotyped behaviour and, hence, can be used as a good model for investigating the general mechanisms underlying olfactory navigation.…”

mentioning

confidence: 99%

Information flow through neural circuits for pheromone orientation

et al. 2014

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Moths use a sophisticated olfactory navigation strategy for resource localization. Here we investigate the neuronal circuits involved in sensory processing to generate locomotor commands for pheromone-source orientation in the moth. We identify a candidate pathway for pheromone processing in the protocerebrum using a mass-staining technique. Our intracellular recordings of pheromone responsiveness detect four major circuits, including a newly identified unstructured neuropil, the superior medial protocerebrum, which supplies output to the lateral accessory lobe (LAL), the premotor centre for walking commands. Interneurons innervating the lower division of the LAL elicited longer responses than those innervating the upper division. Descending interneurons innervating the lower division of the LAL showed a state-dependent flip-flop response. In contrast, input from other visual areas in the protocerebrum mostly converge onto the upper division of the LAL. These results reveal the basic organization of the LAL: the upper division is identified as a protocerebral hub that receives inputs from various areas, while the lower division generates long-lasting activity for locomotor command.

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Rats track odour trails accurately using a multi-layered strategy with near-optimal sampling

Cited by 103 publications

References 35 publications

Intermediate intrinsic diversity enhances neural population coding

Intermediate intrinsic diversity enhances neural population coding

Laterality and Symmetry in Rat Olfactory Behavior and in Physiology of Olfactory Input

Information flow through neural circuits for pheromone orientation

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