Proprioceptive encoding of head position in the black soldier fly, Hermetia illucens (L.) (Stratiomyidae)

Because the eyes of insects cannot be moved independently of the head, information about head posture is essential for stabilizing the visual world or providing information about the direction of gaze. We examined the external anatomy and physiological capabilities of a head posture proprioceptor, the prosternal organ (PO), located at the base of the neck in the black soldier fly, Hermetia illucens (L.) (Family: Stratiomyidae). The PO is sexually isomorphic and is composed of two fused plates of about 130 mechanosensory hairs set in asymmetrical sockets whose orientation varies across the organ. A multi-joint mechanical coupling between the head, neck membrane, and contact sclerites deflects the hairs more or less to increase or decrease their level of excitation. The PO sensory afferents project to the central nervous system (CNS) via a pair of bilateral prosternal nerves (PN) to the fused thoracic ganglia. Simultaneous recording of spiking activity in the PN and videotaping of wind-induced and voluntary head movements around all three axes of head rotation reveal that a few PN afferents are active at rest, but activity increases tonically in response to head deflections. Activity is significantly modulated by change in head angles around the pitch (+/-40 degrees ), yaw (+/-30 degrees ) and roll (more than +/-90 degrees ) axes, although the dynamic range of spiking activity differs for each axis of rotation. Prosternal nerve afferents are bilaterally excited (inhibited) by pitch down (up); excited (inhibited) by head yaw toward the ipsilateral (contralateral) side; excited by roll down toward the ipsilateral side, but little inhibited by roll toward the opposite side. Although bilateral comparison of activity in PN afferents reliably encodes head posture around a given rotational axis, from the point of view of the CNS, the problem of encoding head posture is ill-posed with three axes of rotation and only two streams of afferent information. Furthermore, when the head is rotated around more than one axis simultaneously, mechanical interactions in the neck modify the responses to postural changes around the three rotational axes, which adds further ambiguity to reliable encoding of head posture. The properties of the PO in this relatively basal fly species are compared to those of higher flies and possible mechanisms of disambiguation are discussed.