Feedback from Network States Generates Variability in a Probabilistic Olfactory Circuit

Gordus, Andrew; Pokala, Navin; Levy, Sagi; Flavell, Steven W.; Bargmann, Cornelia I.

doi:10.1016/j.cell.2015.02.018

Cited by 229 publications

(327 citation statements)

References 60 publications

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“…It remains to be seen whether independent calcium dynamics in the processes are unique to these few specific neurons or are a more general phenomenon. For example, a recent investigation of three C. elegans interneurons found that calcium activity peaked more quickly in the process than the cell body but was otherwise similar (29). Although it is tempting to try to explore neural dynamics in the processes by expressing a calcium indicator in the cytoplasm of all neurons, pan-neuronal cytoplasmic expression of a fluorophore is impractical for segmenting individual processes.…”

Section: Discussionmentioning

confidence: 99%

See 1 more Smart Citation

Whole-brain calcium imaging with cellular resolution in freely behaving Caenorhabditis elegans

Nguyen

Shipley

Linder

et al. 2015

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

363

355

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The ability to acquire large-scale recordings of neuronal activity in awake and unrestrained animals is needed to provide new insights into how populations of neurons generate animal behavior. We present an instrument capable of recording intracellular calcium transients from the majority of neurons in the head of a freely behaving Caenorhabditis elegans with cellular resolution while simultaneously recording the animal's position, posture, and locomotion. This instrument provides whole-brain imaging with cellular resolution in an unrestrained and behaving animal. We use spinning-disk confocal microscopy to capture 3D volumetric fluorescent images of neurons expressing the calcium indicator GCaMP6s at 6 head-volumes/s. A suite of three cameras monitor neuronal fluorescence and the animal's position and orientation. Custom software tracks the 3D position of the animal's head in real time and two feedback loops adjust a motorized stage and objective to keep the animal's head within the field of view as the animal roams freely. We observe calcium transients from up to 77 neurons for over 4 min and correlate this activity with the animal's behavior. We characterize noise in the system due to animal motion and show that, across worms, multiple neurons show significant correlations with modes of behavior corresponding to forward, backward, and turning locomotion.calcium imaging | large-scale recording | behavior | C. elegans | microscopy H ow do patterns of neural activity generate an animal's behavior? To answer this question, it is important to develop new methods for recording from large populations of neurons in animals as they move and behave freely. The collective activity of many individual neurons appears to be critical for generating behaviors including arm reach in primates (1), song production in zebrafinch (2), the choice between swimming or crawling in leech (3), and decision-making in mice during navigation (4). New methods for recording from larger populations of neurons in unrestrained animals are needed to better understand neural coding of these behaviors and neural control of behavior more generally.Calcium imaging has emerged as a promising technique for recording dynamics from populations of neurons. Calcium-sensitive proteins are used to visualize changes in intracellular calcium levels in neurons in vivo which serve as a proxy for neural activity (5). To resolve the often weak fluorescent signal of an individual neuron in a dense forest of other labeled cells requires a high magnification objective with a large numerical aperture that, consequently, can image only a small field of view. Calcium imaging has traditionally been performed on animals that are stationary from anesthetization or immobilization to avoid imaging artifacts induced by animal motion. As a result, calcium imaging studies have historically focused on small brain regions in immobile animals that exhibit little or no behavior (6).No previous neurophysiological study has attained whole-brain imaging with cellular resolution in a...

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Section: Discussionmentioning

confidence: 99%

“…24 and and then developing rapidly (17,18,(25)(26)(27)(28)(29). One limitation of these freely moving calcium imaging systems is that they are limited to imaging only a very small subset of neurons and lack the ability to distinguish neurons that lie atop one another in the axial direction of the microscope.…”

mentioning

confidence: 99%

Whole-brain calcium imaging with cellular resolution in freely behaving Caenorhabditis elegans

Nguyen

Shipley

Linder

et al. 2015

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

363

355

View full text Add to dashboard Cite

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“…Action selection in nematodes is driven by shifts in global brain dynamics (119), and there is sufficient plasticity in the nematode nervous system for their responses to vary with system state (120). However, there is no evidence that nematodes can actively hunt for things beyond their immediate sensory environment.…”

Section: Beyond Insectsmentioning

confidence: 99%

What insects can tell us about the origins of consciousness

Barron

Klein

2016

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

263

183

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How, why, and when consciousness evolved remain hotly debated topics. Addressing these issues requires considering the distribution of consciousness across the animal phylogenetic tree. Here we propose that at least one invertebrate clade, the insects, has a capacity for the most basic aspect of consciousness: subjective experience. In vertebrates the capacity for subjective experience is supported by integrated structures in the midbrain that create a neural simulation of the state of the mobile animal in space. This integrated and egocentric representation of the world from the animal's perspective is sufficient for subjective experience. Structures in the insect brain perform analogous functions. Therefore, we argue the insect brain also supports a capacity for subjective experience. In both vertebrates and insects this form of behavioral control system evolved as an efficient solution to basic problems of sensory reafference and true navigation. The brain structures that support subjective experience in vertebrates and insects are very different from each other, but in both cases they are basal to each clade. Hence we propose the origins of subjective experience can be traced to the Cambrian. subjective experience | primary consciousness | vertebrate midbrain | central complex

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“…Thus, one interesting possibility is that olfactory and mechanosensory information about food availability converge at the level of premotor and motor neurons. Notably, recent work demonstrates the activity state of some premotor interneurons downstream of chemosensory neurons can have profound effects on neural responses to odors, 21 providing an additional avenue by which peptide modulation of premotor and motor activity may shape local search responses.…”

Section: The Interneuron Dva and Local Search Behaviormentioning

confidence: 99%

In the proper context: Neuropeptide regulation of behavioral transitions during food searching

Bhattacharya

Francis

2015

Worm

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Feedback from Network States Generates Variability in a Probabilistic Olfactory Circuit

Cited by 229 publications

References 60 publications

Whole-brain calcium imaging with cellular resolution in freely behaving Caenorhabditis elegans

Whole-brain calcium imaging with cellular resolution in freely behaving Caenorhabditis elegans

What insects can tell us about the origins of consciousness

In the proper context: Neuropeptide regulation of behavioral transitions during food searching

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