The Neuroanatomical Ultrastructure and Function of a Biological Ring Attractor

Turner-Evans, Daniel B.; Jensen, Kristopher T.; Ali, Saba; Paterson, Tyler; Sheridan, Arlo; Ray, Robert P.; Wolff, Tanya; Lauritzen, J. Scott; Rubin, Gerald M.; Bock, Davi D.; Jayaraman, Vivek

doi:10.1016/j.neuron.2020.08.006

Cited by 99 publications

(198 citation statements)

References 101 publications

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“…7F,G). In R4m terminals in the EB, the distribution of tunings is less uniform still, hinting at subcellular processes which may impact R4m signalling locally in the EB, a computational motif for which there is precedence both in the CX and in visual neurons generally (Franconville et al, 2018;Turner-Evans et al, 2020;Yang et al, 2016). As a consequence, it appears that the ensemble activity of R4m synapses could convey a preferential response for a particular angle of polarization to columnar neurons at any location in the EB.…”

Section: Populations Of R4m Ring Neurons Exhibit a Preferred Angle Ofmentioning

confidence: 99%

“…Could each of these have differential responses to polarized light to enable different configurations across the PB? Intriguingly, the TB1-like 7 neurons in the Drosophila PB appear to synapse onto only a subset of the E-PG neurons in a single glomerulus (Turner-Evans et al, 2020), perhaps indicating independent functional groups. We may therefore yet find a polarotopic organization of responses in the Drosophila CX.…”

Section: Sensory Transformations Through the Avpmentioning

confidence: 99%

“…A comparative approach would therefore provide insight into the processing strategies employed across taxa as well as species-specific adaptations (Honkanen et al, 2019). Furthermore, it may be possible to reconcile the existing evidence of a common, fixed representation of polarization patterns in the CX of non-Dipteran insects (Heinze and Homberg, 2007;Heinze and Reppert, 2011;Stone et al, 2017) with the emerging model of a flexible representation of both visual information and heading direction in the Drosophila CX (Fisher et al, 2019;Kim et al, 2017Kim et al, , 2019Seelig and Jayaraman, 2015;Turner-Evans et al, 2020). Alternatively, fundamental differences in the organization and processing of polarized light signals between species may reflect specialized navigational requirements.…”

Section: Introductionmentioning

confidence: 99%

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A visual pathway for skylight polarization processing inDrosophila

Hardcastle

Omoto

Kandimalla

et al. 2020

Preprint

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SUMMARYMany insects use patterns of polarized light in the sky to orient and navigate. Here we functionally characterize neural circuitry in the fruit fly, Drosophila melanogaster, that conveys polarized light signals from the eye to the central complex, a brain region essential for the fly’s sense of direction. Neurons tuned to the angle of polarization of ultraviolet light are found throughout the anterior visual pathway, connecting the optic lobes with the central complex via the anterior optic tubercle and bulb, in a homologous organization to the ‘sky compass’ pathways described in other insects. We detail how a consistent, map-like organization of neural tunings in the peripheral visual system is transformed into a reduced representation suited to flexible processing in the central brain. This study identifies computational motifs of the transformation, enabling mechanistic comparisons of multisensory integration and central processing for navigation in the brains of insects.

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Section: Populations Of R4m Ring Neurons Exhibit a Preferred Angle Ofmentioning

confidence: 99%

Section: Sensory Transformations Through the Avpmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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A visual pathway for skylight polarization processing inDrosophila

Hardcastle

Omoto

Kandimalla

et al. 2020

Preprint

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“…The compass neurons are part of a recurrent sub-network with a topological and dynamical resemblance to theorized network structures called ring attractors (Ben-Yishai et al, 1995) that have been hypothesized to compute head direction in the mammalian brain (Hulse and Jayaraman, 2019;Kim et al, 2017b;Turner-Evans et al, 2017;Turner-Evans et al, 2020;Xie et al, 2002;Zhang, 1996). A key connection in the sub-network is from the compass neurons to a population of interneurons in a handlebar-shaped structure called the protocerebral bridge (PB) ( Figure 1C).…”

Section: Introductionmentioning

confidence: 99%

“…The context-dependent initiation and control of many such behaviors is thought to depend on a highly conserved insect brain region called the central complex (CX) (Figure 1, Figure 1-figure supplement 1, Figure 2) (Helfrich-Forster, 2018;Pfeiffer and Homberg, 2014;Strauss, 2002;Turner-Evans and Jayaraman, 2016). In Drosophila, this highly recurrent central brain region, which is composed of ~3000 identified neurons, enables flies to modulate their locomotor activity by time of day (Liang et al, 2019), maintain an arbitrary heading when flying (Giraldo et al, 2018;Warren et al, 2018) and walking (Green et al, 2019;Turner-Evans et al, 2020), form short-and long-term visual memories that aid in spatial navigation (Kuntz et al, 2017;Liu et al, 2006;Neuser et al, 2008;Ofstad et al, 2011), use internal models of their body size when performing motor tasks (Krause et al, 2019), track sleep need and induce sleep (Donlea et al, 2018), and consolidate memories during sleep (Dag et al, 2019).…”

Section: Introductionmentioning

confidence: 99%

A connectome of theDrosophilacentral complex reveals network motifs suitable for flexible navigation and context-dependent action selection

Hulse

Haberkern

Franconville

et al. 2020

Preprint

Self Cite

138

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Flexible behaviors over long timescales are thought to engage recurrent neural networks in deep brain regions, which are experimentally challenging to study. In insects, recurrent circuit dynamics in a brain region called the central complex (CX) enable directed locomotion, sleep, and context- and experience-dependent spatial navigation. We describe the first complete electron-microscopy-based connectome of the Drosophila CX, including all its neurons and circuits at synaptic resolution. We identified new CX neuron types, novel sensory and motor pathways, and network motifs that likely enable the CX to extract the fly’s head-direction, maintain it with attractor dynamics, and combine it with other sensorimotor information to perform vector-based navigational computations. We also identified numerous pathways that may facilitate the selection of CX-driven behavioral patterns by context and internal state. The CX connectome provides a comprehensive blueprint necessary for a detailed understanding of network dynamics underlying sleep, flexible navigation, and state-dependent action selection.

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Distribution and daily oscillation of GABA in the circadian system of the cockroach Rhyparobia maderae

Massah

Neupert

Brodesser

et al. 2021

J of Comparative Neurology

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Gamma-aminobutyric acid (GABA) is the prevalent inhibitory neurotransmitter in nervous systems promoting sleep in both mammals and insects. In the Madeira cockroach, sleep-wake cycles are controlled by a circadian clock network in the brain's optic lobes, centered in the accessory medulla (AME) with its innervating pigment-dispersing factor (PDF) expressing clock neurons at the anterior-ventral rim of the medulla. GABA is present in cell clusters that innervate different circuits of the cockroach's AME clock, without colocalizing in PDF clock neurons. Physiological, immunohistochemical, and behavioral assays provided evidence for a role of GABA in light entrainment, possibly via the distal tract that connects the AME's glomeruli to the medulla. Furthermore, GABA was implemented in clock outputs to multiple effector systems in optic lobe and midbrain. Here, GABAergic brain circuits were analyzed further, focusing on the circadian system in search for sleep/wake controlling brain circuits. All GABAimmunoreactive neurons of the cockroach brain were also stained with an antiserum against the GABA-synthesizing enzyme glutamic acid decarboxylase. We found strong overlap of the distribution of GABA-immunoreactive networks with PDF clock networks in optic lobes and midbrain. Neurons in five of the six soma groups that innervate the clock exhibited GABA immunoreactivity. The intensity of GABA immunoreactivity in the distal tract showed daily fluctuations with maximum staining intensity in the middle of the day and weakest staining at the end of the day. Quantification via enzyme-linked immunosorbent assay and quantitative liquid chromatography coupled to electrospray ionization tandem mass spectrometry, likewise, showed higher GABA levels in the optic lobe during the inactivity phase of the cockroach during the day and lower levels during its activity phase at dusk. Our data further support the hypothesis that light-and PDF-dependently the circadian clock network of the cockroach controls GABA levels and thereby promotes sleep during the day.

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The Neuroanatomical Ultrastructure and Function of a Biological Ring Attractor

Cited by 99 publications

References 101 publications

A visual pathway for skylight polarization processing inDrosophila

A visual pathway for skylight polarization processing inDrosophila

A connectome of theDrosophilacentral complex reveals network motifs suitable for flexible navigation and context-dependent action selection

Distribution and daily oscillation of GABA in the circadian system of the cockroach Rhyparobia maderae

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