Structure and kinematics of the prosternal organs and their influence on head position in the blowfly Calliphora erythrocephala Meig.

Abstract

The blowfly Calliphora has a mobile head and various, presumably proprioceptive, sense organs in the neck region. The "prosternal organs" are a pair of mechanosensory hair fields, each comprising ca. 110 sensilla. We studied their structure (Figs. 2-4), kinematics (Figs. 5, 6) and, after surgery, their influence on head posture in order to reveal their specific function.The hair sensilla are structurally polarized, all in roughly the same direction, and are stimulated by dorsoventral bending of the hairs (Figs. 3, 4). This occurs indirectly by flap-movements of two contact sclerites (Figs. 3, 6); they move in the same direction during pitch turns of the head, in opposite directions during roll turns, and barely at all during yaw turns of the head (Fig. 5).Bending and arresting all hairs of one field elicits a head roll bias to the non-operated side (Fig. 7) during tethered flight in visually featureless surroundings. In contrast, shaving all hairs of one field elicits a head roll to the operated side . The surgically induced bias of head posture is not compensated within three days (Fig. 10). Our results show that the prosternal organs of Calliphora sense pitch and roll turns of the fly's head, and control at least its roll position.Abbreviations." HP ~ TP ~ angular positions of the sagittal planes of the fly's head and thorax, respectively, relative to an external reference; HR~ head roll angle of the fly's head relative to its thorax, HR>0 ~ for clockwise head roll, looking in flight direction; N, number of flies; n, number of measurements; PO, prosternal organ; SD, standard deviation; SEM, standard error of the mean * Present address:

Visual gaze control during peering flight manoeuvres in honeybees

“…A similar relationship was also observed in tethered flying locusts, flies and dragonflies, where a turn of the head evokes active thorax rotation (Mittelstaedt 1950;Goodman 1965;Liske 1977). The control systems that coordinate head and thorax orientation (recently reviewed in Taylor & Krapp 2007) break down after deafferentation of cervical mechanosensors, demonstrating the essential role of proprioceptive information for this posture reflex (Mittelstaedt 1950;Goodman 1965;Preuss & Hengstenberg 1992;Gilbert & Bauer 1998;Gilbert & Kim 2007). Bees do possess proprioceptive hair plates in the neck region, which could be used to measure the relative orientation between the head and the thorax (Lindauer & Nedel 1959;Markl 1962).…”

Nonlinear Integration of Visual and Haltere Inputs in Fly Neck Motor Neurons

“…It is probable that the visual responses of type II NMNs are gated not exclusively by the halteres but also by other sensory inputs such as those from the proprioceptive prosternal organ (Preuss and Hengstenberg, 1992 Nonlinear multisensory integration at motor neurons may explain behavioral results. A simple schematic illustrates the agreement between our electrophysiological results and previous behavioral findings.…”

Behavioural evidence for a visual and proprioceptive control of head roll in hoverflies (Episyrphus balteatus, Dipteran)

“…The halteres form a mechanosensory gyroscopic system that is sensitive to Coriolis forces (Nalbach, 1993;Hengstenberg, 1993Hengstenberg, , 1998Huston and Krapp, 2009) and measure the rotational speed of the body during fast perturbations or manoeuvres and drive opposite head roll movements (Schwyn et al, 2011). An example of proprioceptive structure, the prosternal organs, consisting of a pair of mechanosensitive hair fields located symmetrically on the neck on the anterior part of the thorax of insects (Pringle, 1938;Preuss and Hengstenberg, 1992;Paulk and Gilbert, 2006), are stimulated by the head position through 'contact sclerites' (Peters, 1962). Differential stimulation of opposite sclerites during head roll movements generates mechanoreceptive cues about the head-inbody roll orientation (Preuss and Hengstenberg, 1992).…”

“…An example of proprioceptive structure, the prosternal organs, consisting of a pair of mechanosensitive hair fields located symmetrically on the neck on the anterior part of the thorax of insects (Pringle, 1938;Preuss and Hengstenberg, 1992;Paulk and Gilbert, 2006), are stimulated by the head position through 'contact sclerites' (Peters, 1962). Differential stimulation of opposite sclerites during head roll movements generates mechanoreceptive cues about the head-inbody roll orientation (Preuss and Hengstenberg, 1992). Although the mechanosensory sensors located on the neck are involved in compensatory reflex responses realigning the head with the body in flies (Horn and Lang, 1978;Preuss and Hengstenberg, 1992) and are connected neuroanatomically to an insect's neck motor system (Strausfeld and Seyan, 1985;Milde et al, 1987), the exact contribution of these sensors to head control during flight has not yet been clearly established.…”