An Anatomically Constrained Model for Path Integration in the Bee Brain

Thomas Stone, Barbara Webb, Andrea Adden, Nicolai Ben Weddig, Anna Honkanen, Rachel Templin, William Wcislo, Luca Scimeca, Eric Warrant, Stanley Heinze
2017 Current Biology  
6 Path integration is a widespread navigational strategy in which directional changes and distance 7 covered are continuously integrated on an outward journey, enabling a straight-line return to 8 home. Bees use vision for this taska celestial-cue based visual compass, and an optic-flow 9 based visual odometerbut the underlying neural integration mechanisms are unknown. Using 10 intracellular electrophysiology, we show that polarized-light based compass-neurons and optic-11 flow-based
more » ... ding neurons converge in the central complex of the bee brain, and 12 through block-face electron microscopy we identify potential integrator cells. Based on plausible 13 output targets for these cells, we propose a complete circuit for path integration and steering in 14 the central complex, with anatomically-identified neurons suggested for each processing step. 15 The resulting model-circuit is thus fully constrained biologically and provides a functional 16 interpretation for many previously unexplained architectural features of the central complex. 17 Moreover, we show that the receptive fields of the newly discovered speed neurons can support 18 path integration for the holonomic motion (i.e. a ground velocity that is not precisely aligned 19 2 with body orientation) typical of bee-flight, a feature not captured in any previously proposed 20 model of path integration. In a broader context, the model-circuit presented provides a general 21 mechanism for producing steering signals by comparing current and desired headings -22 suggesting a more basic function for central-complex connectivity from which path integration 23 may have evolved. 24 25 28 3 variety of sensory environments, suggesting that the underlying neural mechanisms are both 42 robust and conserved. However, despite rich behavioral data, the neural basis of path integration 43 in bees, or insects in general, is unknown, although several hypothetical circuits have been 44 proposed (reviewed and compared in [5]). One region of the insect brain that plays a prominent 45 role in orientation behaviors is the central complex (CX), a conglomerate of highly conserved 46 brain compartments [6]. In migratory locusts and fruit flies this region houses an ordered array of 47 4 CX via a highly conserved neural pathway [10,11], which, in locusts, has been shown to produce 64 an ordered array of compass neurons, suited to encode heading in a global reference frame due to 65 the fixed relation between E-vector angle and solar azimuth [7]. In flies, homologous cells also 66 encode head direction, suggesting that mapping of directional space in the CX is a shared feature 67 across insects [8,12]. These cells encode head-direction based on visual landmark cues, but are 68 also updated by self-motion cues in the absence of vision [8], a finding recently confirmed in 69 cockroach head-direction cells [13]. As bees possess specialized eye regions for perceiving 70 polarized light [14,15] and use a polarized-light based compass during foraging, we first ask 71 whether polarized-light based compass neurons also exist in the bee CX (Figure 1). For 72 physiological recordings, we focused on the CX of the tropical nocturnal bee Megalopta genalis 73 [16] (Figure 1A). These bees forage at times of the day when polarized skylight provides the 74 single most reliable directional cue in their rainforest habitat and they possess all optical 75 specializations typical for polarized-light perception [15]. Bees were captured with light traps 76 directly from their natural habitat in Panama during foraging flights and tested within two weeks 77 of capture. We successfully recorded from 160 Megalopta bees to test responses of CX-neurons 78 to linearly polarized light (Figure 1B-H) by continuously rotating an artificial sky above the 79 animal ( Figure 1C -E). We found strong sinusoidal modulations of firing frequency in response to 80 this stimulus (i.e. polarized-light tuning) in ten neurons. The neurons showed an average tuning 81 width of 50˚ and a difference in tuning between clockwise and counter-clockwise rotations of 53˚ 82 on average, with anticipatory tuning optima, i.e., during clockwise rotations the optimum was 83 shifted counter-clockwise with respect to the average tuning and vice versa for counter-84 clockwise rotations ( Figure 1E-H) . This phenomenon has been found in compass neurons of 85 other species and, in locusts, has been proposed to aid correct compass encoding during fast 86 5 body rotations [17]. None of the cells tested (5 out of 10 cells) responded strongly to large-field 87 motion cues presented in a 360˚ LED arena and showed no or only weak responses to a bright 88 bar moving around the bee (tested in 9 out of 10 cells), demonstrating that the recorded neurons 89 are selectively encoding polarized-light based compass cues ( Figure S1 ). Seven compass neurons 90 were analyzed anatomically. All arborized in the lower division of the central body (ellipsoid 91 body in flies; Figure 1B ), a part of the CX tightly associated with compass encoding in migratory 92 insects and a key component of the Drosophila head direction network [8,10,11]. Indeed, both 93 identified neuron types with compass-like activity in Megalopta (6x TL, and 1x CL1-neurons) 94 are either homologous to the GABAergic (inhibitory) ring-neurons or to the E-PG-neurons that 95 comprise the head direction system of the Drosophila CX. These cells make up an estimated 5-96 10% of all CX-neurons and identical neurons have been described in detail in locusts [18,19], 97 monarch butterflies [10] and dung beetles [20] with physiological responses to polarized light 98 that are highly similar to those in Megalopta. Additionally, we identified bee-counterparts of all 99 remaining locust compass neurons, occupying the protocerebral bridge (PB) (TB1-neurons; 100 anatomically identified) and the upper division of the central body (CBU, fan-shaped body in 101 flies) (CPU1-neurons; anatomy and physiology) (Figure 1B, S4). Together these findings 102 strongly suggest that the CX serves as an internal compass in bees as well. 103 104 Optic flow sensing in the bee CX 105 The second requirement for path integration is an odometer, which for the bee requires neurons 106 that encode translational information from optic flow to converge with visual compass 107 information [4]. Recent evidence from Drosophila and cockroaches shows that the CX houses 108 neurons sensitive to large-field motion cues [21][22][23]. During intracellular recordings from CX-109 6 neurons we presented large-field optic flow stimuli (high-contrast sinewave gratings moving at 110 different speeds) to bees located in the center of a 360˚ LED arena (Figure 2A ). Two types of 111 CX-neurons responded strongly to translational optic flow, whereas they were invariant to 112 compass stimuli (tested in 5 of 14 recordings; Figure S1 ). Both selectively provided input to two 113
doi:10.1016/j.cub.2017.08.052 pmid:28988858 pmcid:PMC6196076 fatcat:puozzf75d5e5ximui55dwzajqe