Journal of Neurophysiology, Vol 69, Issue 2 329-339, Copyright © 1993 by APS

ARTICLES

Neural circuit tuning fly visual interneurons to motion of small objects. I. Dissection of the circuit by pharmacological and photoinactivation techniques

A. K. Warzecha, M. Egelhaaf and A. Borst
Max-Planck-Institut fur biologische Kybernetik, Tubingen, Germany.

1. Visual interneurons tuned to the motion of small objects are found in many animal species and are assumed to be the neuronal basis of figure-ground discrimination by relative motion. A well-examined example is the FD1-cell in the third visual neuropil of blowflies. This cell type responds best to motion of small objects. Motion of extended patterns elicits only small responses. As a neuronal mechanism that leads to such a response characteristic, it was proposed that the FD1-cell is inhibited by the two presumably GABAergic and, thus, inhibitory CH-cells, the VCH- and the DCH-cell. The CH-cells respond best to exactly that type of motion by which the activity of the FD1-cell is reduced. The hypothesis that the CH-cells inhibit the FD1-cell and, thus, mediate its selectivity to small moving objects was tested by ablating the CH-cells either pharmacologically or by photoinactivation. 2. After application of the gamma-aminobutyric acid (GABA) antagonist picrotoxinin, the FD1-cell responds more strongly to large-field than to small-field motion, i.e., it has lost its small-field selectivity. This suggests that the tuning of the FD1-cell to small moving objects relies on a GABAergic mechanism and, thus, most likely on the CH-cells. 3. The role of each CH-cell for small-field tuning was determined by inactivating them individually. They were injected with a fluorescent dye and then ablated by laser illumination. Only photoinactivation of the VCH-cell eliminated the specific selectivity of the FD1-cell for small-field motion. Ablation of the DCH-cell did not significantly change the response characteristic of the FD1-cell. This reveals the important role of the VCH-cells in mediating the characteristic sensitivity of the FD1-cell to motion of small objects. 4. The FD1-cell is most sensitive to motion of small objects in the ventral part of the ipsilateral visual field, whereas motion in the dorsal part influences the cell only weakly. This specific feature fits well to the sensitivity of the VCH-cell to ipsilateral motion that is most pronounced in the ventral part of the visual field. The spatial sensitivity distribution of the FD1-cell matches also the characteristics of figure-ground discrimination and fixation behavior.

This article has been cited by other articles:

				J. Grewe, N. Matos, M. Egelhaaf, and A.-K. Warzecha Implications of Functionally Different Synaptic Inputs for Neuronal Gain and Computational Properties of Fly Visual Interneurons J Neurophysiol, October 1, 2006; 96(4): 1838 - 1847. [Abstract] [Full Text] [PDF]

				K. Karmeier, J. H. van Hateren, R. Kern, and M. Egelhaaf Encoding of Naturalistic Optic Flow by a Population of Blowfly Motion-Sensitive Neurons J Neurophysiol, September 1, 2006; 96(3): 1602 - 1614. [Abstract] [Full Text] [PDF]

				R. Kern, J. H. van Hateren, and M. Egelhaaf Representation of behaviourally relevant information by blowfly motion-sensitive visual interneurons requires precise compensatory head movements J. Exp. Biol., April 1, 2006; 209(7): 1251 - 1260. [Abstract] [Full Text] [PDF]

				P. Neri Spatial Integration of Optic Flow Signals in Fly Motion-Sensitive Neurons J Neurophysiol, March 1, 2006; 95(3): 1608 - 1619. [Abstract] [Full Text] [PDF]

				F. Gabbiani, I. Cohen, and G. Laurent Time-Dependent Activation of Feed-Forward Inhibition in a Looming-Sensitive Neuron J Neurophysiol, September 1, 2005; 94(3): 2150 - 2161. [Abstract] [Full Text] [PDF]

				K. Karmeier, H. G. Krapp, and M. Egelhaaf Population Coding of Self-Motion: Applying Bayesian Analysis to a Population of Visual Interneurons in the Fly J Neurophysiol, September 1, 2005; 94(3): 2182 - 2194. [Abstract] [Full Text] [PDF]

				J. H. van Hateren, R. Kern, G. Schwerdtfeger, and M. Egelhaaf Function and Coding in the Blowfly H1 Neuron during Naturalistic Optic Flow J. Neurosci., April 27, 2005; 25(17): 4343 - 4352. [Abstract] [Full Text] [PDF]

				R. Kurtz Ca2+ Clearance in Visual Motion-Sensitive Neurons of the Fly Studied In Vivo by Sensory Stimulation and UV Photolysis of Caged Ca2+ J Neurophysiol, July 1, 2004; 92(1): 458 - 467. [Abstract] [Full Text] [PDF]

				J. Grewe, J. Kretzberg, A.-K. Warzecha, and M. Egelhaaf Impact of Photon Noise on the Reliability of a Motion-Sensitive Neuron in the Fly's Visual System J. Neurosci., November 26, 2003; 23(34): 10776 - 10783. [Abstract] [Full Text] [PDF]

				K. Farrow, J. Haag, and A. Borst Input Organization of Multifunctional Motion-Sensitive Neurons in the Blowfly J. Neurosci., October 29, 2003; 23(30): 9805 - 9811. [Abstract] [Full Text] [PDF]

				H. Cuntz, J. Haag, and A. Borst Neural image processing by dendritic networks PNAS, September 16, 2003; 100(19): 11082 - 11085. [Abstract] [Full Text] [PDF]

				J. Haag and A. Borst Dendro-Dendritic Interactions between Motion-Sensitive Large-Field Neurons in the Fly J. Neurosci., April 15, 2002; 22(8): 3227 - 3233. [Abstract] [Full Text] [PDF]

				R. Kurtz, A.-K. Warzecha, and M. Egelhaaf Transfer of Visual Motion Information via Graded Synapses Operates Linearly in the Natural Activity Range J. Neurosci., September 1, 2001; 21(17): 6957 - 6966. [Abstract] [Full Text] [PDF]

				H. G. Krapp, R. Hengstenberg, and M. Egelhaaf Binocular Contributions to Optic Flow Processing in the Fly Visual System J Neurophysiol, February 1, 2001; 85(2): 724 - 734. [Abstract] [Full Text] [PDF]

				R. Kurtz, V. Durr, and M. Egelhaaf Dendritic Calcium Accumulation Associated With Direction-Selective Adaptation in Visual Motion-Sensitive Neurons In Vivo J Neurophysiol, October 1, 2000; 84(4): 1914 - 1923. [Abstract] [Full Text] [PDF]

				V. Durr and M. Egelhaaf In Vivo Calcium Accumulation in Presynaptic and Postsynaptic Dendrites of Visual Interneurons J Neurophysiol, December 1, 1999; 82(6): 3327 - 3338. [Abstract] [Full Text] [PDF]

				A Warzecha, W Horstmann, and M Egelhaaf Temperature-dependence of neuronal performance in the motion pathway of the blowfly calliphora erythrocephala J. Exp. Biol., January 11, 1999; 202(22): 3161 - 3170. [Abstract] [PDF]

				H. G. Krapp, B. Hengstenberg, and R. Hengstenberg Dendritic Structure and Receptive-Field Organization of Optic Flow Processing Interneurons in the Fly J Neurophysiol, April 1, 1998; 79(4): 1902 - 1917. [Abstract] [Full Text] [PDF]

				R. M. Glantz Directionality and Inhibition in Crayfish Tangential Cells J Neurophysiol, March 1, 1998; 79(3): 1157 - 1166. [Abstract] [Full Text] [PDF]