Abstract
The lobula giant movement detector (LGMD) is a large-field visual interneuron believed to be involved in collision avoidance and escape behaviors in orthopteran insects, such as locusts. Responses to approaching—or looming—stimuli are highly stereotypical, producing a peak that signals an angular size threshold. Over the past several decades, investigators have elucidated many of the mechanisms underpinning this response, demonstrating that the LGMD implements a multiplication in log-transformed coordinates. Furthermore, the LGMD possesses several mechanisms that preclude it responding to non-looming stimuli. This chapter explores these biophysical mechanisms, as well as highlighting insights the LGMD provides into general principles of dendritic integration.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Bacon JP, Thompson KS, Stern M (1995) Identified octopaminergic neurons provide an arousal mechanism in the locust brain. J Neurophysiol 74:2739–2743
Baden T, Hedwig B (2007) Neurite-specific Ca2+ dynamics underlying sound processing in an auditory interneurone. Dev Neurobiol 67:68–80
Bernander O, Douglas RJ, Martin KA, Koch C (1991) Synaptic background activity influences spatiotemporal integration in single pyramidal cells. Proc Natl Acad Sci USA 88:11569–11573
Bollmann JH, Engert F (2009) Subcellular topography of visually driven dendritic activity in the vertebrate visual system. Neuron 61:895–905
Borst A, Egelhaaf M (1992) In vivo imaging of calcium accumulation in fly interneurons as elicited by visual motion stimulation. Proc Natl Acad Sci USA 89:4139–4143
Borst A, Haag J, Reiff DF (2010) Fly motion vision. Annu Rev Neurosci 33:49–70
Branco T, Clark BA, Häusser M (2010) Dendritic discrimination of temporal input sequences in cortical neurons. Science 329:1671–1675
Burrows M, Rowell CHF (1973) Connections between descending visual interneurons and metathoracic motoneurons in the locust. J Comp Physiol 85:221–234
Dewell RB, Gabbiani F (2012) Role of active conductances for dendritic processing in a looming sensitive neuron. Poster presented at the Society for Neuroscience, New Orleans, 13–17 October 2012
Douglass JK, Strausfeld NJ (2003) Retinotopic pathways providing motion-selective information to the lobula from peripheral elementary motion-detecting circuits. J Comp Neurol 457:326–344
Fotowat H, Gabbiani F (2007) Relationship between the phases of sensory and motor activity during a looming-evoked multistage escape behavior. J Neurosci 27:10047–10059
Fotowat H, Gabbiani F (2011) Collision detection as a model for sensory-motor integration. Annu Rev Neurosci 34:1–19
Fotowat H, Harrison RR, Gabbiani F (2011) Multiplexing of motor information in the discharge of a collision detecting neuron during escape behaviors. Neuron 69:147–158
Gabbiani F, Cohen I, Laurent G (2005) Time-dependent activation of feed-forward inhibition in a looming-sensitive neuron. J Neurophysiol 94:2150–2161
Gabbiani F, Krapp HG (2006) Spike-frequency adaptation and intrinsic properties of an identified, looming-sensitive neuron. J Neurophysiol 96:2951–2962
Gabbiani F, Krapp HG, Hatsopoulos N, Mo CH, Koch C, Laurent G (2004) Multiplication and stimulus invariance in a looming-sensitive neuron. J Physiol Paris 98:19–34
Gabbiani F, Krapp HG, Koch C, Laurent G (2002) Multiplicative computation in a visual neuron sensitive to looming. Nature 420:320–324
Gabbiani F, Krapp HG, Laurent G (1999) Computation of object approach by a wide-field, motion-sensitive neuron. J Neurosci 19:1122–1141
Gabbiani F, Mo C, Laurent G (2001) Invariance of angular threshold computation in a wide-field looming-sensitive neuron. J Neurosci 21:314–329
Guest BB, Gray JR (2006) Responses of a looming-sensitive neuron to compound and paired object approaches. J Neurophysiol 95:1428–1441
Hatsopoulos N, Gabbiani F, Laurent G (1995) Elementary computation of object approach by wide-field visual neuron. Science 270:1000–1003
Hille B (2001) Ionic channels of excitable membranes. Sinauer Associates, Sunderland, MA
James AC, Osorio D (1996) Characterisation of columnar neurons and visual signal processing in the medulla of the locust optic lobe by system identification techniques. J Comp Physiol A 178:183–199
Joesch M, Schnell B, Raghu SV, Reiff DF, Borst A (2010) ON and OFF pathways in Drosophila motion vision. Nature 468:300–304
Johnston D, Magee JC, Colbert CM, Cristie BR (1996) Active properties of neuronal dendrites. Annu Rev Neurosci 19:165–186
Johnston D, Wu SM (1995) Foundations of cellular neurophysiology. Bradford Books, New York, NY
Jones PW, Gabbiani F (2010) Synchronized neural input shapes stimulus selectivity in a collision-detecting neuron. Curr Biol 20:2052–2057
Jones PW, Gabbiani F (2012) Logarithmic compression of sensory signals within the dendritic tree of a collision-sensitive neuron. J Neurosci 32:4923–4934
Judge S, Rind F (1997) The locust DCMD, a movement-detecting neuron tightly tuned to collision trajectories. J Exp Biol 200:2209–2216
Judkewitz B, Rizzi M, Kitamura K, Häusser M (2009) Targeted single-cell electroporation of mammalian neurons in vivo. Nat Protoc 4:862–869
Jung SN, Borst A, Haag J (2011) Flight activity alters velocity tuning of fly motion-sensitive neurons. J Neurosci 31:9231–9237
Killmann F, Gras H, Schürmann F (1999) Types, numbers and distribution of synapses on the dendritic tree of an identified visual interneuron in the brain of the locust. Cell Tissue Res 296:645–665
Killmann F, Schürmann FW (1985) Both electrical and chemical transmission between the lobula giant movement detector and the descending contralateral movement detector neurons of locusts are supported by electron microscopy. J Neurocytol 14:637–652
Koch C, Poggio T, Torre V (1983) Nonlinear interactions in a dendritic tree: localization, timing, and role in information processing. Proc Natl Acad Sci USA 80:2799–2802
Krapp HG, Gabbiani F (2005) Spatial distribution of inputs and local receptive field properties of a wide-field, looming sensitive neuron. J Neurophysiol 93:2240–2253
Liang P, Kern R, Kurtz R, Egelhaaf M (2011) Impact of visual motion adaptation on neural responses to objects and its dependence on the temporal characteristics of optic flow. J Neurophysiol 105:1825–1834
London M, Häusser M (2005) Dendritic computation. Annu Rev Neurosci 28:503–532
Magee JC (1999) Dendritic lh normalizes temporal summation in hippocampal CA1 neurons. Nat Neurosci 2:508–514
Magee JC (2000) Dendritic integration of excitatory synaptic input. Nat Rev Neurosci 1:181–190
O’Shea M (1975) Two sites of axonal spike initiation in a bimodal interneuron. Brain Res 96:93–98
O’Shea M, Rowell CHF (1975a) A spike-transmitting electrical synapse between visual interneurons in the locust movement detector system. J Comp Physiol 97:143–158
O’Shea M, Rowell CHF (1975b) Protection from habituation by lateral inhibition. Nature 254:53–55
O’Shea M, Rowell CHF (1976) The neuronal basis of a sensory analyser, the acridid movement detector system. II. Response decrement, convergence, and the nature of the excitatory afferents to the fan-like dendrites of the LGMD. J Exp Biol 65:289–308
O’Shea M, Rowell CHF, Williams JLD (1974) The anatomy of a locust visual interneurone: the descending contralateral movement detector. J Exp Biol 60:1–12
O’Shea M, Williams JLD (1974) The anatomy and output connection of a locust visual interneurone: the lobular giant movement detector (LGMD) neuron. J Comp Physiol 91:257–266
Ogawa H, Cummins GI, Jacobs GA, Miller JP (2006) Visualization of ensemble activity patterns of mechanosensory afferents in the cricket cercal sensory system with calcium imaging. J Neurobiol 66:293–307
Ogawa H, Cummins GI, Jacobs GA, Oka K (2008) Dendritic design implements algorithm for synaptic extraction of sensory information. J Neurosci 28:4592–4603
Palka J (1967) An inhibitory process influencing visual responses in a fibre of the ventral nerve cord of locusts. J Insect Physiol 13:235–248
Peron SP, Gabbiani F (2009a) Spike frequency adaptation mediates looming stimulus selectivity in a collision-detecting neuron. Nat Neurosci 12:318–326
Peron SP, Gabbiani F (2009b) Role of spike-frequency adaptation in shaping neuronal response to dynamic stimuli. Biol Cybern 100:505–520
Peron SP, Jones PW, Gabbiani F (2009) Precise subcellular input retinotopy and its computational consequences in an identified visual interneuron. Neuron 63:830–842
Peron SP, Krapp HG, Gabbiani F (2007) Influence of electrotonic structure and synaptic mapping on the receptive field properties of a collision-detecting neuron. J Neurophysiol 97:159–177
Petreanu L, Mao T, Sternson SM, Svoboda K (2009) The subcellular organization of neocortical excitatory connections. Nature 457:1142–1145
Rall W (1967) Distinguishing theoretical synaptic potentials computed for different soma-dendritic distributions of synaptic input. J Neurophysiol 30:1138–1168
Rall W, Burke RE, Smith TG, Nelson PG, Frank K (1967) Dendritic location of synapses and possible mechanisms for the monosynaptic EPSP in motoneurons. J Neurophysiol 30:1169–1193
Reichardt W (1987) Computation of optical motion by movement detectors. Biophys Chem 26:263–278
Rind FC (1984) A chemical synapse between two motion detecting neurones in the locust brain. J Exp Biol 110:143–167
Rind FC, Leitinger G (2000) Immunocytochemical evidence that collision sensing neurons in the locust visual system contain acetylcholine. J Comp Neurol 423:389–401
Rind FC, Santer RD, Wright GA (2008) Arousal facilitates collision avoidance mediated by a looming sensitive visual neuron in a flying locust. J Neurophysiol 100:670–680
Rind FC, Simmons PJ (1992) Orthopteran DCMD neuron: a reevaluation of responses to moving objects. I. Selective responses to approaching objects. J Neurophysiol 68:1654–1666
Rind FC, Simmons PJ (1998) Local circuit for the computation of object approach by an identified visual neuron in the locust. J Comp Neurol 395:405–415
Rogers SM, Krapp HG, Burrows M, Matheson T (2007) Compensatory plasticity at an identified synapse tunes a visuomotor pathway. J Neurosci 27:4621–4633
Rowell CHF (1971) Variable responsiveness of a visual interneurone in the free-moving locust, and its relation to behaviour and arousal. J Exp Biol 55:727–747
Rowell CHF, O’Shea M (1976a) The neuronal basis of a sensory analyser, the acridid movement detector system. I. Effects of simple incremental and decremental stimuli in light and dark adapted animals. J Exp Biol 65:273–288
Rowell CHF, O’Shea M (1976b) Neuronal basis of a sensory analyser, the acridid movement detector system. III. Control of response amplitude by tonic lateral inhibition. J Exp Biol 65:617–625
Rowell CHF, O’Shea M, Williams JLD (1977) The neuronal basis of a sensory analyser, the acridid movement detector system. IV. The preference for small field stimuli. J Exp Biol 68:157–185
Santer RD, Rind FC, Stafford R, Simmons PJ (2006) Role of an identified looming-sensitive neuron in triggering a flying locusts escape. J Neurophysiol 95:3391–3400
Santer RD, Simmons PJ, Rind FC (2005) Gliding behaviour elicited by lateral looming stimuli in flying locusts. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 191:61–73
Santer RD, Yamawaki Y, Rind FC, Simmons PJ (2008) Preparing for escape: an examination of the role of the DCMD neuron in locust escape jumps. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 194:69–77
Schlotterer GR (1977) Response of the locust descending movement detector neuron to rapidly approaching and withdrawing visual stimuli. Can J Zool 55:1372–1376
Segev I, London M (2000) Untangling dendrites with quantitative models. Science 290:744–750
Silver RA (2010) Neuronal arithmetic. Nat Rev Neurosci 11:474–489
Simmons PJ (1980) Connexions between a movement-detecting visual interneurone and flight motoneurons of a locust. J Exp Biol 86:87–97
Simmons PJ, Rind FC (1992) Orthopteran DCMD neuron: a reevaluation of responses to moving objects. II. Critical cues for detecting approaching objects. J Neurophysiol 68:1667–1682
Single S, Borst A (2002) Different mechanisms of calcium entry within different dendritic compartments. J Neurophysiol 87:1616–1624
Single S, Haag J, Borst A (1997) Dendritic computation of direction selectivity and gain control in visual interneurons. J Neurosci 17:6023–6030
Spruston N (2008) Pyramidal neurons: dendritic structure and synaptic integration. Nat Rev Neurosci 11:1059–1067
Strausfeld NJ, Nässel DR (1981) Neuroarchitectures serving compound eyes of crustacea and insects. In: Autrum H (ed) Handbook of sensory physiology, vol VII/68. Springer, Berlin
Stuart G, Spruston N, Häusser M (2008) Dendrites. Oxford University Press, New York, NY
Tsien RY (1980) New calcium indicators and buffers with high selectivity against magnesium and protons: design, synthesis, and properties of prototype structures. Biochemistry 19:2396–2404
Zador AM, Agmon-Snir H, Segev I (1995) The morphoelectrotonic transform: a graphical approach to dendritic function. J Neurosci 15:1669–1682
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2014 Springer Science+Business Media New York
About this chapter
Cite this chapter
Peron, S.P. (2014). Biophysical Mechanisms of Computation in a Looming Sensitive Neuron. In: Cuntz, H., Remme, M., Torben-Nielsen, B. (eds) The Computing Dendrite. Springer Series in Computational Neuroscience, vol 11. Springer, New York, NY. https://doi.org/10.1007/978-1-4614-8094-5_17
Download citation
DOI: https://doi.org/10.1007/978-1-4614-8094-5_17
Published:
Publisher Name: Springer, New York, NY
Print ISBN: 978-1-4614-8093-8
Online ISBN: 978-1-4614-8094-5
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)