Neural mechanisms underlying fundamental vertebrate motor activities can be usefully studies in model systems from other phyla which offer the advantage of a limited number of neurons accessible to intracellular techniques and modern structural analysis. One such activity, generically known as the oculomotor response, comprises complex patterns of behaviour mediated by the visual and vestibular systems: gaze, object scanning and fixation, and the stabilization of the retinal image compensating for complex spatial displacements of the head and body. Oculomotor abnormalities in humans can indicate the onset of central nervous trauma and disease. A greater understanding of the cellular organization of a complex multisensory oculomotor pathway could provide useful leads and suggestions for research on the physiologically less accessible vertebrate counterpart. One such model is provided by the dipteran Calliphora erythrocephala, which has a wide range of sophisticated oculomotor behaviours. In both sexes panoramic motion elicits compensatory head and body movements. Objects is visual space elicit fixation and orientation behaviour. In Calliphora there is a profound sexual dimorphism of the eye: in males there are more receptors, a zone of high visual acuity, and unique sex-specific neurons in the visual centers. Only males are able to sustain fixation, tracking and interception of small rapidly moving objects. This is distinct from behaviour shared by both sexes in which panoramic flow fields are computed by elemental motion- detectors and relayed to giant tectal neurons. Ultimately, mechanosensory information, derived from strategically placed organs for balance tactile perception is integrated with visual information in discrete brain centers from which originate 1) descending pathways to thoracic motor centers controlling head and body musculature and 2) interneurons supplying cerebellarlike higher centers in the midbrain. This research will employ intracellular recordings and stainings, and sophisticated light and electron microscopical strategies to dissect the cellular organization of identified nerve cells, from the receptors to the motor neurons and musculature. The research will focus on the following: 1) retinotopic organization and multimodal response characteristics of visual interneurons; 2) intracellular recordings and synaptic relationships of descending motor neurons; 3) innervation, physiology, and dynamics of effector muscles; 4) skeletal attachment, arthrology, and behaviour. This research proposes to broaden our understanding of neural mechanisms involved in visuo-mechanosensory control of eye movements. A complete description of motor control in this model will contribute a major step towards understanding circuitry for complex oculomotor behaviour and the role of uniquely identified neurons in visual pursuit and interception.

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National Eye Institute (NEI)
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Visual Sciences B Study Section (VISB)
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University of Arizona
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Strausfeld, N J; Kong, A; Milde, J J et al. (1995) Oculomotor control in calliphorid flies: GABAergic organization in heterolateral inhibitory pathways. J Comp Neurol 361:298-320
Gilbert, C; Gronenberg, W; Strausfeld, N J (1995) Oculomotor control in calliphorid flies: head movements during activation and inhibition of neck motor neurons corroborate neuroanatomical predictions. J Comp Neurol 361:285-97
Gronenberg, W; Milde, J J; Strausfeld, N J (1995) Oculomotor control in calliphorid flies: organization of descending neurons to neck motor neurons responding to visual stimuli. J Comp Neurol 361:267-84
Strausfeld, N J; Barth, F G (1993) Two visual systems in one brain: neuropils serving the secondary eyes of the spider Cupiennius salei. J Comp Neurol 328:43-62
Strausfeld, N J; Weltzien, P; Barth, F G (1993) Two visual systems in one brain: neuropils serving the principal eyes of the spider Cupiennius salei. J Comp Neurol 328:63-75
Strausfeld, N J; Gilbert, C (1992) Small-field neurons associated with oculomotor control in muscoid flies: cellular organization in the lobula plate. J Comp Neurol 316:56-71
Gronenberg, W; Strausfeld, N J (1992) Premotor descending neurons responding selectively to local visual stimuli in flies. J Comp Neurol 316:87-103
Gilbert, C; Strausfeld, N J (1992) Small-field neurons associated with oculomotor and optomotor control in muscoid flies: functional organization. J Comp Neurol 316:72-86
Gronenberg, W; Strausfeld, N J (1991) Descending pathways connecting the male-specific visual system of flies to the neck and flight motor. J Comp Physiol A 169:413-26
Gilbert, C; Strausfeld, N J (1991) The functional organization of male-specific visual neurons in flies. J Comp Physiol A 169:395-411

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