Experience- and Context-Dependent Modulation of the Invertebrate Compass System
Authors: Timothy A. Currier, Katherine I. Nagel
Journal: Neuron (2020)

How are head direction signals computed and maintained in neural circuits? In this issue of Neuron, Shiozaki et al., 2020Shiozaki H.M. Ohta K. Kazama H. A Multi-regional Network Encoding Heading and Steering Maneuvers in Drosophila.Neuron. 2020; 106 (this issue): 126-141Abstract Full Text Full Text PDF PubMed Scopus (23) Google Scholar expand our understanding of the fly “compass” network, revealing context- and experience-dependent changes in the multiplexed encoding of head direction and steering maneuvers. How are head direction signals computed and maintained in neural circuits? In this issue of Neuron, Shiozaki et al., 2020Shiozaki H.M. Ohta K. Kazama H. A Multi-regional Network Encoding Heading and Steering Maneuvers in Drosophila.Neuron. 2020; 106 (this issue): 126-141Abstract Full Text Full Text PDF PubMed Scopus (23) Google Scholar expand our understanding of the fly “compass” network, revealing context- and experience-dependent changes in the multiplexed encoding of head direction and steering maneuvers. One of the main jobs of the brain is to move an animal through space. Perhaps it is not surprising, then, that representations of an animal’s orientation and movement through space are widespread in the brain. Although the existence of such representations in vertebrates has been known for over a decade, the more recent discovery of heading direction selectivity in fruit fly neurons has made it possible to study the circuit mechanisms that generate these signals. In a landmark paper, Seelig and Jayaraman, 2015Seelig J.D. Jayaraman V. Neural dynamics for landmark orientation and angular path integration.Nature. 2015; 521: 186-191Crossref PubMed Scopus (371) Google Scholar first showed that a group of neurons in the fly Central Complex (CX)—so-called “compass” cells or E-PGs (Figure 1)—contains a representation of head direction. A “bump” of calcium activity moves through a ring of these neurons as the fly turns. The strength and position of this E-PG bump depend on both visual cues and the fly’s own movements. A few years later, two groups reported the discovery of P-EN cells (Green et al., 2017Green J. Adachi A. Shah K.K. Hirokawa J.D. Magani P.S. Maimon G. A neural circuit architecture for angular integration in Drosophila.Nature. 2017; 546: 101-106Crossref PubMed Scopus (148) Google Scholar, Turner-Evans et al., 2017Turner-Evans D. Wegener S. Rouault H. Franconville R. Wolff T. Seelig J.D. Druckmann S. Jayaraman V. Angular velocity integration in a fly heading circuit.eLife. 2017; 6: e23496Crossref PubMed Scopus (128) Google Scholar) that encode angular velocity and rotate the E-PG heading bump. P-ENs provide a mechanism by which the fly can integrate its own movements to maintain an estimate of orientation in space. This process is thought to be critical for tasks such as path integration, where an animal keeps track of its orientation and distance relative to a nest after a long and circuitous outbound route (Stone et al., 2017Stone T. Webb B. Adden A. Weddig N.B. Honkanen A. Templin R. Wcislo W. Scimeca L. Warrant E. Heinze S. An Anatomically Constrained Model for Path Integration in the Bee Brain.Curr. Biol. 2017; 27: 3069-3085.e11Abstract Full Text Full Text PDF PubMed Scopus (161) Google Scholar). More recent modeling and connectomics studies support the hypothesis that the E-PG compass functions as a ring attractor, allowing it to select a single heading estimate despite complex visual input (Kim et al., 2017Kim S.S. Rouault H. Druckmann S. Jayaraman V. Ring attractor dynamics in the Drosophila central brain.Science. 2017; 356: 849-853Crossref PubMed Scopus (156) Google Scholar). E-PGs and P-ENs are found in the ellipsoid body (EB), just one of many neuropils that make up the ancient and evolutionarily conserved CX. The fan-shaped body (FB), another CX neuropil, is anatomically similar to the EB. It possesses CX-intrinsic columnar neurons, akin to E-PGs and P-ENs, and tangential cells that provide extrinsic input. A prominent hypothesis in the field has been that FB columns function similarly to the columns of the EB, with activity in FB columnar neurons representing either heading or angular velocity. In this issue of Neuron, new work from Shiozaki et al., 2020Shiozaki H.M. Ohta K. Kazama H. A Multi-regional Network Encoding Heading and Steering Maneuvers in Drosophila.Neuron. 2020; 106 (this issue): 126-141Abstract Full Text Full Text PDF PubMed Scopus (23) Google Scholar tests this hypothesis directly. To examine whether FB columns also encode orientation, Shiozaki and colleagues monitored the wingbeat amplitude of tethered flies while recording calcium activity in subsets of FB columnar neurons. By comparing the stroke amplitude of the left and right wings, intended turning behavior was used to rotate a visual panorama, giving the fly sensory feedback consistent with having actually made a turn. This “closed loop” stimulus allows flies to navigate in a reduced virtual environment. Under these conditions, Shiozaki et al., 2020Shiozaki H.M. Ohta K. Kazama H. A Multi-regional Network Encoding Heading and Steering Maneuvers in Drosophila.Neuron. 2020; 106 (this issue): 126-141Abstract Full Text Full Text PDF PubMed Scopus (23) Google Scholar found that the middle layers of the FB encode heading direction. Importantly, coordinated activity was observed across the EB and FB, suggesting that both populations of columnar neurons carry related signals. Under pan-neuronal GCaMP expression, ventral FB layers did not represent orientation, even though a columnar structure is present there. These data largely support the hypothesis that FB columns operate similarly to and coordinately with EB columns, with some layer-specific exceptions. Shiozaki et al., 2020Shiozaki H.M. Ohta K. Kazama H. A Multi-regional Network Encoding Heading and Steering Maneuvers in Drosophila.Neuron. 2020; 106 (this issue): 126-141Abstract Full Text Full Text PDF PubMed Scopus (23) Google Scholar also found responses that are inconsistent with, or even directly contradictory to, previous work. For example, whereas a previous study found that E-PGs do not encode turns in darkness during flight (Kim et al., 2017Kim S.S. Rouault H. Druckmann S. Jayaraman V. Ring attractor dynamics in the Drosophila central brain.Science. 2017; 356: 849-853Crossref PubMed Scopus (156) Google Scholar), this study found that they do. Further, Shiozaki et al., 2020Shiozaki H.M. Ohta K. Kazama H. A Multi-regional Network Encoding Heading and Steering Maneuvers in Drosophila.Neuron. 2020; 106 (this issue): 126-141Abstract Full Text Full Text PDF PubMed Scopus (23) Google Scholar found that FB columns represent not only orientation but angular velocity as well. Indeed, CX columns on the whole (including those in the EB) appear to encode turn rate more strongly than orientation. In contrast to previous work (Seelig and Jayaraman, 2015Seelig J.D. Jayaraman V. Neural dynamics for landmark orientation and angular path integration.Nature. 2015; 521: 186-191Crossref PubMed Scopus (371) Google Scholar), representations of orientation were found to decay, quickly drifting away from reality. What could account for this difference? To explore this question, Shiozaki et al., 2020Shiozaki H.M. Ohta K. Kazama H. A Multi-regional Network Encoding Heading and Steering Maneuvers in Drosophila.Neuron. 2020; 106 (this issue): 126-141Abstract Full Text Full Text PDF PubMed Scopus (23) Google Scholar mimicked the short-trial design of Kim et al., 2017Kim S.S. Rouault H. Druckmann S. Jayaraman V. Ring attractor dynamics in the Drosophila central brain.Science. 2017; 356: 849-853Crossref PubMed Scopus (156) Google Scholar and compared these results to their long-trial data. The authors found that the details of prior stimulus exposure had a significant impact on the strength of orientation versus turn-rate encoding in CX columnar neurons. This exciting result suggests that learning, or some form of state-dependent modulation, is capable of altering CX representation on the order of tens of seconds. This result is consistent with recent work from Fisher et al., 2019Fisher Y.E. Lu J. D’Alessandro I. Wilson R.I. Sensorimotor experience remaps visual input to a heading-direction network.Nature. 2019; 576: 121-125Crossref PubMed Scopus (66) Google Scholar, who demonstrated that sensory tuning in EB columnar neurons could be modified by experience on similar timescales. In the EB, this plasticity appears to occur at synapses between extrinsic ring neurons and intrinsic columnar neurons. In the FB, synapses between extrinsic inputs and columnar neurons could show similar experience-dependent modulation. Shiozaki et al., 2020Shiozaki H.M. Ohta K. Kazama H. A Multi-regional Network Encoding Heading and Steering Maneuvers in Drosophila.Neuron. 2020; 106 (this issue): 126-141Abstract Full Text Full Text PDF PubMed Scopus (23) Google Scholar also observed shorter timescale modulation of CX columnar neuron responses. In particular, FB columnar neuron branches in the noduli (NO) displayed sensory context-dependent turning signals. With the visual panorama active, left turns activated the right NO and right turns activated the left NO. In darkness, this relationship was reversed but only in FB columnar cells. This neuropil-specific sensory modulation may hint at the FB’s unique contribution to navigation behavior. Finally, Shiozaki et al., 2020Shiozaki H.M. Ohta K. Kazama H. A Multi-regional Network Encoding Heading and Steering Maneuvers in Drosophila.Neuron. 2020; 106 (this issue): 126-141Abstract Full Text Full Text PDF PubMed Scopus (23) Google Scholar also found that the turn-related activity they observed in FB neurons was most strongly correlated with steering maneuvers, rather than angular velocity per se. In closed-loop, turning-related motor activity and changes in the visual scene are coupled, so it is difficult to disentangle which is being encoded by a neural response. To discriminate between these possibilities, the authors altered the gain of visual feedback, similar to experiments first performed by Seelig and Jayaraman, 2015Seelig J.D. Jayaraman V. Neural dynamics for landmark orientation and angular path integration.Nature. 2015; 521: 186-191Crossref PubMed Scopus (371) Google Scholar. However, whereas Seelig and Jayaraman found that E-PG activity mostly followed the visual scene, Shiozaki et al., 2020Shiozaki H.M. Ohta K. Kazama H. A Multi-regional Network Encoding Heading and Steering Maneuvers in Drosophila.Neuron. 2020; 106 (this issue): 126-141Abstract Full Text Full Text PDF PubMed Scopus (23) Google Scholar found that activity in P-FRs, a group of FB neurons, followed wing maneuvers. They observed a similar but non-significant effect in E-PGs. Whether these encoding differences are cell-type specific or related to an animal’s sensorimotor experience will have to be resolved by future experiments. Although the discovery of head direction cells in flies has allowed for major progress in understanding the mechanisms by which heading representations are computed, the functional relevance of this representation is still unclear. Large lesions of the CX result in navigational defects (Strauss and Heisenberg, 1993Strauss R. Heisenberg M. A higher control center of locomotor behavior in the Drosophila brain.J. Neurosci. 1993; 13: 1852-1861Crossref PubMed Google Scholar), but the effects of targeted silencing are more subtle. Multiple groups have shown that silencing compass neurons impairs the ability of flies to maintain a fixed offset to a visual landmark but does not disrupt visual object fixation per se (Giraldo et al., 2018Giraldo Y.M. Leitch K.J. Ros I.G. Warren T.L. Weir P.T. Dickinson M.H. Sun Navigation Requires Compass Neurons in Drosophila.Curr. Biol. 2018; 28: 2845-2852.e4Abstract Full Text Full Text PDF PubMed Scopus (72) Google Scholar). One model proposes that FB columnar neurons integrate speed and orientation information to encode a memory of the home vector during path integration (Stone et al., 2017Stone T. Webb B. Adden A. Weddig N.B. Honkanen A. Templin R. Wcislo W. Scimeca L. Warrant E. Heinze S. An Anatomically Constrained Model for Path Integration in the Bee Brain.Curr. Biol. 2017; 27: 3069-3085.e11Abstract Full Text Full Text PDF PubMed Scopus (161) Google Scholar). Directly testing this hypothesis will require more complex, 2D navigation behaviors (Haberkern et al., 2019Haberkern H. Basnak M.A. Ahanonu B. Schauder D. Cohen J.D. Bolstad M. Bruns C. Jayaraman V. Visually Guided Behavior and Optogenetically Induced Learning in Head-Fixed Flies Exploring a Virtual Landscape.Curr. Biol. 2019; 29: 1647-1659.e8Abstract Full Text Full Text PDF PubMed Scopus (29) Google Scholar). The work of Shiozaki et al., 2020Shiozaki H.M. Ohta K. Kazama H. A Multi-regional Network Encoding Heading and Steering Maneuvers in Drosophila.Neuron. 2020; 106 (this issue): 126-141Abstract Full Text Full Text PDF PubMed Scopus (23) Google Scholar represents a significant advance to our understanding of navigation control, in both the hypotheses that it supports and the nuances it exposes. FB columns do represent heading direction but only in some layers. FB activity is coordinated with EB activity, but the variable most strongly represented can be turn rate, not orientation. FB representations are stable over short timescales but are affected by stimulus history over longer ones. NO branch activity is similar in EB and FB columnar cells, but not under varied sensory contexts. These exceptions and clarifications form the body of this work’s contributions, providing clues toward determining how each CX neuropil uniquely controls and modulates navigation. A Multi-regional Network Encoding Heading and Steering Maneuvers in DrosophilaShiozaki et al.NeuronFebruary 4, 2020In BriefThe central complex of Drosophila plays key roles in navigational behavior. Using cell-type-specific calcium imaging during flight, Shiozaki et al. show that heading direction and turning behavior are encoded in distributed networks of neurons in this brain region. Full-Text PDF Open Archive