Representation of Haltere Oscillations and Integration with Visual Inputs in the Fly Central Complex

Abstract

The reduced hindwings of flies, known as halteres, are specialized mechanosensory organs that detect body rotations during flight. Primary afferents of the haltere encode its oscillation frequency linearly over a wide bandwidth and with precise phase-dependent spiking. However, it is not currently known whether information from haltere primary afferent neurons is sent to higher brain centers where sensory information about body position could be used in decision making, or whether precise spike timing is useful beyond the peripheral circuits that drive wing movements. We show that in cells in the central brain, the timing and rates of neural spiking can be modulated by sensory input from experimental haltere movements (driven by a servomotor). Using multichannel extracellular recording in restrained flesh flies (Sarcophaga bullata of both sexes), we examined responses of central complex cells to a range of haltere oscillation frequencies alone, and in combination with visual motion speeds and directions. Haltere-responsive units fell into multiple response classes, including those responding to any haltere motion and others with firing rates linearly related to the haltere frequency. Cells with multisensory responses showed higher firing rates than the sum of the unisensory responses at higher haltere frequencies. They also maintained visual properties, such as directional selectivity, while increasing response gain nonlinearly with haltere frequency. Although haltere inputs have been described extensively in the context of rapid locomotion control, we find haltere sensory information in a brain region known to be involved in slower, higher-order behaviors, such as navigation.Many animals use vision for navigation; however, these cues must be interpreted in the context of the body's position. In mammalian brains, hippocampal cells combine visual and vestibular information to encode head direction. A region of the arthropod brain, known as the central complex (CX), similarly encodes heading information, but it is unknown whether proprioceptive information is integrated here as well. We show that CX neurons respond to input from halteres, specialized proprioceptors in flies that detect body rotations. These neurons also respond to visual input, providing one of the few examples of multiple sensory modalities represented in individual CX cells. Haltere stimulation modifies neural responses to visual signals, providing a mechanism for integrating vision with proprioception.

Encoding and control of orientation to airflow by a set of Drosophila fan-shaped body neurons

“…Although previous studies have examined CX responses to a wide variety of sensory cues ( Heinze and Homberg, 2007 ; Weir and Dickinson, 2015 ; Ritzmann et al, 2008 ; Phillips-Portillo, 2012 ; Kathman and Fox, 2019 ), it has remained unclear to what extent these responses are organized or specialized across CX compartments. By targeting specific cell populations using genetic driver lines, the present study supports the hypothesis that distinct cell types within the CX represent specific sensory cues.…”

“…As in the EB, FB neurons represent a wide array of sensory cues, including optic flow, polarized light, and mechanical activation of the antennae or halteres ( Weir and Dickinson, 2015 ; Heinze et al, 2009 ; Ritzmann et al, 2008 ; Phillips-Portillo, 2012 ; Kathman and Fox, 2019 ). Although it has received less attention than vision or olfaction, flow of the air or water is a critical mechanosensory cue for animals navigating in aquatic, terrestrial, and air-borne environments ( Montgomery et al, 1997 ; Yu et al, 2016a ; Alerstam et al, 2011 ; Reynolds et al, 2010 ).…”

Encoding and control of airflow orientation by a set ofDrosophilafan-shaped body neurons

“…Although previous studies have examined CX responses to a wide variety of sensory cues (Heinze and Homberg 2007;Weir and Dickinson, 2015;Ritzmann et al, 2008;Phillips-Portillo, 2012;Kathman and Fox, 2019), it has remained unclear to what extent these responses are organized or specialized across CX compartments. By targeting specific cell populations using genetic driver lines, the present study supports the hypothesis that distinct cell types within the CX represent specific sensory cues.…”

“…As in the EB, FB neurons represents a wide array of sensory cues, including optic flow, polarized light, and mechanical activation of the antennae or halteres (Weir and Dickinson, 2015;Heinze et al 2009, Ritzmann et al, 2008Phillips-Portillo, 2012;Kathman and Fox, 2019). Although it has received less attention than vision or olfaction, flow of the air or water is a critical mechanosensory cue for animals navigating in aquatic, terrestrial, and air-borne environments (Montgomery et al, 1997;Yu et al, 2016a;Alerstam et al, 2011;Reynolds et al, 2010).…”

Takeoff diversity in Diptera

“…The neural mechanism by which the halteres would contribute to takeoff strategy is still unclear. Direct connections between the haltere nerve and the legs have not been identified, but haltere information is represented in the brain [42] and indirect connections through the frontal nerve and thoracic ganglion have been shown to exist [43]. One possibility is that haltere activation could contribute to a CNS 'warm-up' prior to the initiation of flight.…”