Cellular Basis of Head Direction and Contextual Cues in the Insect Brain

Varga, Angelika; Ritzmann, Roy E.

doi:10.1016/j.cub.2016.05.037

Cited by 78 publications

(94 citation statements)

References 51 publications

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“…Neurons that maintain such a representation in darkness have been reported across various species (Knierim and Zhang, 2012; Seelig and Jayaraman, 2015; Taube et al, 1990; Varga and Ritzmann, 2016). Several computational models have been proposed to explain how a population representation of heading might be updated using angular velocity signals from different neural populations, but identifying connections between neurons that carry and integrate these disparate signals has been challenging in mammals (Knierim and Zhang, 2012).…”

Section: Discussionmentioning

confidence: 99%

Angular velocity integration in a fly heading circuit

Turner-Evans

Wegener

Rouault

et al. 2017

eLife

267

453

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Many animals maintain an internal representation of their heading as they move through their surroundings. Such a compass representation was recently discovered in a neural population in the Drosophila melanogaster central complex, a brain region implicated in spatial navigation. Here, we use two-photon calcium imaging and electrophysiology in head-fixed walking flies to identify a different neural population that conjunctively encodes heading and angular velocity, and is excited selectively by turns in either the clockwise or counterclockwise direction. We show how these mirror-symmetric turn responses combine with the neurons’ connectivity to the compass neurons to create an elegant mechanism for updating the fly’s heading representation when the animal turns in darkness. This mechanism, which employs recurrent loops with an angular shift, bears a resemblance to those proposed in theoretical models for rodent head direction cells. Our results provide a striking example of structure matching function for a broadly relevant computation.DOI: http://dx.doi.org/10.7554/eLife.23496.001

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Section: Discussionmentioning

confidence: 99%

Angular velocity integration in a fly heading circuit

Turner-Evans

Wegener

Rouault

et al. 2017

eLife

267

453

View full text Add to dashboard Cite

show abstract

“…Indeed, the head-direction activity bump drifted out of sync with the real heading of the fly in darkness. By measuring the activity of individual neurons with extracellular recordings rather than imaging an entire neuronal population, head-direction cells resembling those in the fly were found also in cockroaches [98]. …”

Section: The Neural Basis Of Path Integrationmentioning

confidence: 99%

Principles of Insect Path Integration

2018

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Continuously monitoring its position in space relative to a goal is one of the most essential tasks for an animal that moves through its environment. Species as diverse as rats, bees, and crabs achieve this by integrating all changes of direction with the distance covered during their foraging trips, a process called path integration. They generate an estimate of their current position relative to a starting point, enabling a straight-line return, following what is known as a home vector. While in theory path integration always leads the animal precisely back home, in the real world noise limits the usefulness of this strategy when operating in isolation. Noise results from stochastic processes in the nervous system and from unreliable sensory information, particularly when obtaining heading estimates. Path integration, during which angular self-motion provides the sole input for encoding heading (idiothetic path integration), results in accumulating errors that render this strategy useless over long distances. In contrast, when using an external compass this limitation is avoided (allothetic path integration). Many navigating insects indeed rely on external compass cues for estimating body orientation, whereas they obtain distance information by integration of steps or optic-flow-based speed signals. In the insect brain, a region called the central complex plays a key role for path integration. Not only does the central complex house a ring-attractor network that encodes head directions, neurons responding to optic flow also converge with this circuit. A neural substrate for integrating direction and distance into a memorized home vector has therefore been proposed in the central complex. We discuss how behavioral data and the theoretical framework of path integration can be aligned with these neural data.

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“…We further extended the results from the fly experiments by adopting some of the classical methods used in rat head direction cell studies and applying them in our experiments on cockroach CX function (Varga and Ritzmann, 2016). We used extracellular recordings to gain insight into how single neurons in the CX might contribute to the head direction signal and to draw more direct comparisons between the neural strategies underlying rodent and insect head direction coding.…”

Section: The Neural Substrates Of Navigation In the CXmentioning

confidence: 99%

“…Maximum average firing rates (Hz) of the example units are marked in the right bottom corner of each panel. Modified with permission from Varga and Ritzmann (2016). …”

Section: The Neural Substrates Of Navigation In the CXmentioning

confidence: 99%

Spatial Navigation and the Central Complex: Sensory Acquisition, Orientation, and Motor Control

Varga

Kathman

Martin

et al. 2017

Front. Behav. Neurosci.

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Cockroaches are scavengers that forage through dark, maze-like environments. Like other foraging animals, for instance rats, they must continually asses their situation to keep track of targets and negotiate barriers. While navigating a complex environment, all animals need to integrate sensory information in order to produce appropriate motor commands. The integrated sensory cues can be used to provide the animal with an environmental and contextual reference frame for the behavior. To successfully reach a goal location, navigational cues continuously derived from sensory inputs have to be utilized in the spatial guidance of motor commands. The sensory processes, contextual and spatial mechanisms, and motor outputs contributing to navigation have been heavily studied in rats. In contrast, many insect studies focused on the sensory and/or motor components of navigation, and our knowledge of the abstract representation of environmental context and spatial information in the insect brain is relatively limited. Recent reports from several laboratories have explored the role of the central complex (CX), a sensorimotor region of the insect brain, in navigational processes by recording the activity of CX neurons in freely-moving insects and in more constrained, experimenter-controlled situations. The results of these studies indicate that the CX participates in processing the temporal and spatial components of sensory cues, and utilizes these cues in creating an internal representation of orientation and context, while also directing motor control. Although these studies led to a better understanding of the CX's role in insect navigation, there are still major voids in the literature regarding the underlying mechanisms and brain regions involved in spatial navigation. The main goal of this review is to place the above listed findings in the wider context of animal navigation by providing an overview of the neural mechanisms of navigation in rats and summarizing and comparing our current knowledge on the CX's role in insect navigation to these processes. By doing so, we aimed to highlight some of the missing puzzle pieces in insect navigation and provide a different perspective for future directions.

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Cellular Basis of Head Direction and Contextual Cues in the Insect Brain

Cited by 78 publications

References 51 publications

Angular velocity integration in a fly heading circuit

Angular velocity integration in a fly heading circuit

Principles of Insect Path Integration

Spatial Navigation and the Central Complex: Sensory Acquisition, Orientation, and Motor Control

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