Types, numbers and distribution of synapses on the dendritic tree of an identified visual interneuron in the brain of the locust

Peron SP, Krapp HG, Gabbiani F. Influence of electrotonic structure and synaptic mapping on the receptive field properties of a collision-detecting neuron. J Neurophysiol 97: 159 -177, 2007. First Published October 4, 2006 doi:10.1152/jn.00660.2006. The lobula giant movement detector (LGMD) is a visual interneuron of Orthopteran insects involved in collision avoidance and escape behavior. The LGMD possesses a large dendritic field thought to receive excitatory, retinotopic projections from the entire compound eye. We investigated whether the LGMD's receptive field for local motion stimuli can be explained by its electrotonic structure and the eye's anisotropic sampling of visual space. Five locust (Schistocerca americana) LGMD neurons were stained and reconstructed. We show that the excitatory dendritic field and eye can be fitted by ellipsoids having similar geometries. A passive compartmental model fit to electrophysiological data was used to demonstrate that the LGMD is not electrotonically compact. We derived a spike rate to membrane potential transform using intracellular recordings under visual stimulation, allowing direct comparison between experimental and simulated receptive field properties. By assuming a retinotopic mapping giving equal weight to each ommatidium and equally spaced synapses, the model reproduced the experimental data along the eye equator, though it failed to reproduce the receptive field along the ventral-dorsal axis. Our results illustrate how interactions between the distribution of synaptic inputs and the electrotonic properties of neurons contribute to shaping their receptive fields.

“…1B. Some of these axon terminals contact the DCMD neuron (Killmann et al 1999;. The two inhibitory dendritic fields (B and C in Fig.…”

Section: R E S U L T Smentioning

confidence: 94%

mentioning

confidence: 99%

Influence of Electrotonic Structure and Synaptic Mapping on the Receptive Field Properties of a Collision-Detecting Neuron

Peron

Krapp

Gabbiani

2007

“…Another possible explanation of sublinear summation could involve accurate transmission of information between the LGMD and DCMD. Faithful transferral of LGMD spikes to the DCMD at firing rates Յ400 spikes/s (Rind 1984) occurs via mixed electrical and chemical synapses (Killman et al 1999;O'Shea and Williams 1974), suggesting that sublinear summation is not mediated through this specific pathway. However, further experiments would determine if fidelity across this synapse is maintained at the high spike rates reported here and elsewhere (Money et al 2005).…”

Section: Sublinear Summation Of Multiple Looming Stimulimentioning

confidence: 99%

“…LGMD spikes are transferred to the DCMD in a 1:1 manner (O'Shea and Rowell 1975a;Rind 1984) via mixed electrical and chemical synapses (Killman et al 1999;O'Shea and Williams 1974). Subsequently, the DCMD connects to flight interneurons and motorneurons within the thoracic ganglia (Burrows and Rowell 1973;Robertson and Pearson 1983;Simmons 1980).…”

Section: Introductionmentioning

confidence: 99%

Responses of a Looming-Sensitive Neuron to Compound and Paired Object Approaches

Guest

Gray²

2006

Guest, Bruce B. and John R. Gray. Responses of a looming sensitive neuron to compound and paired object approaches. J Neurophysiol 95: 1428 -1441, 2006. First published November 30, 2005 doi:10.1152/jn.01037.2005. The lobula giant movement detector (LGMD) and its target neuron, the descending contralateral movement detector (DCMD), constitute a motion-sensitive pathway in the locust visual system that responds preferentially to objects approaching on a collision course.LGMD receptive field properties, anisotropic distribution of local retinotopic inputs across the visual field, and localized habituation to repeated stimuli suggest that this pathway should be sensitive to approaches of individual objects within a complex visual scene. We presented locusts with compound looming objects while recording from the DCMD to test the effects of nonuniform edge expansion on looming responses. We also presented paired objects approaching from different regions of the visual field at nonoverlapping, closely timed and simultaneous approach intervals to study DCMD responses to multiple looming stimuli. We found that looming compound objects evoked characteristic responses in the DCMD and that the time of peak firing was consistent with predicted values based on a weighted ratio of the half size of each distinct object edge and the absolute approach velocity. We also found that the azimuthal position and interval of paired approaches affected DCMD firing properties and that DCMDs responded to individual objects approaching within 106 ms of each other. Moreover, comparisons between individual and paired approaches revealed that overlapping approaches are processed in a strongly sublinear manner. These findings are consistent with biophysical mechanisms that produce nonlinear integration of excitatory and feed-forward inhibitory inputs onto the LGMD that have been shown to underlie responses to looming stimuli.

“…It projects onto a postsynaptic target neuron called the descending contralateral movement detector (DCMD) that can easily be recorded from the animal's nerve cord (O'Shea and Williams 1974). The connection between the LGMD and DCMD is mediated by a mixed chemical/electrical synapse (Killmann et al 1999) and is so strong that spikes in the LGMD and DCMD are in a 1:1 correspondence under visual stimulation (Gabbiani et al 2005;O'Shea and Williams 1974;Rind 1984). The LGMD can thus be conveniently identified electrophysiologically as the unique neuron in the optic lobe whose spikes precede by nearly 2 ms those of the DCMD.…”

mentioning

confidence: 99%

Spike-Frequency Adaptation and Intrinsic Properties of an Identified, Looming-Sensitive Neuron

Gabbiani

Krapp²

2006

Gabbiani, Fabrizio and Holger G. Krapp. Spike-frequency adaptation and intrinsic properties of an identified, looming-sensitive neuron. J Neurophysiol 96: 2951-2962, 2006. First published March 29, 2006 doi:10.1152/jn.00075.2006. We investigated in vivo the characteristics of spike-frequency adaptation and the intrinsic membrane properties of an identified, looming-sensitive interneuron of the locust optic lobe, the lobula giant movement detector (LGMD). TheLGMD had an input resistance of 4 -5 M⍀, a membrane time constant of about 8 ms, and exhibited inward rectification and rebound spiking after hyperpolarizing current pulses. Responses to depolarizing current pulses revealed the neuron's intrinsic bursting properties and pronounced spike-frequency adaptation. The characteristics of adaptation, including its time course, the attenuation of the firing rate, the mutual dependency of these two variables, and their dependency on injected current, closely followed the predictions of a model first proposed to describe the adaptation of cat visual cortex pyramidal neurons in vivo. Our results thus validate the model in an entirely different context and suggest that it might be applicable to a wide variety of neurons across species. Spike-frequency adaptation is likely to play an important role in tuning the LGMD and in shaping the variability of its responses to visual looming stimuli.