Subcellular mapping of dendritic activity in optic flow processing neurons

Abstract

i AbstractDendritic integration is a fundamental element of neuronal information processing.So far, few studies have provided a detailed picture of this process, describing the properties of local dendritic activity and its subcellular organization.Here, I used 2--photon calcium imaging in optic flow processing neurons of the blowfly Calliphora vicina to determine the preferred location and direction of local motion cues for small branchlets throughout the entire dendrite. I found a pronounced retinotopic mapping on both the subcellular and the cell population level. In addition, dendritic branchlets residing in different layers of the neuropil were tuned to distinct directions of motion. Within one layer, local preferred directions varied according to the deflections of the ommatidial lattice. Summing the local receptive fields of all dendritic branchlets reproduced the characteristic properties of these neurons' axonal output receptive fields.These results corroborate the notion that the dendritic morphology of vertical system cells allows them to selectively collect local motion inputs with particular directional preferences from a spatially organized input repertoire, thus forming filters that match global patterns of optic flow. These data illustrate a highly structured circuit organization as an efficient way to hard--wire a complex sensory task.

Neural Circuit to Integrate Opposing Motions in the Visual Field

“…Associated with their proposed role as matched filters for sensing the optic flow generated by an animal's self-motion, in contrast to dLGN neurons, lobula plate tangential cells have large receptive fields, in some cases covering more than 100 degrees of visual space (Hopp et al, 2014;Joesch et al, 2008;Krapp and Hengstenberg, 1996;Schnell et al, 2010). Independent movement, e.g., originating from conspecifics or foliage, thus poses a challenge to the system by providing excitatory drive to tangential cells not associated with self-motion.…”

“…Each T4 and T5 cell is tuned to one of four cardinal directions and terminates in one of the four layers of the lobula plate such that opposite directions are represented in adjacent layers (Maisak et al, 2013) (layer 1: front to back; layer 2: back to front; layer 3: upward; layer 4: downward). These directions match the preferred directions of wide-field motion-sensitive tangential cells that extend their dendrites in the respective layers: horizontal system cells with dendrites in layer 1 depolarize during front-to-back motion and hyperpolarize during back-to-front motion, Hx cells in layer 2 exhibit the opposite tuning, and vertical system (VS) cells with dendrites mostly in layer 4 depolarize primarily during downward and hyperpolarize during upward motion (Hausen et al, 1980;Hopp et al, 2014;Schnell et al, 2010;Scott et al, 2002;Wasserman et al, 2015). With T4/T5 cells blocked, tangential cells lose all of their motion sensitivity (Schnell et al, 2012), and flies become completely motion blind .…”

Depth information in natural environments derived from optic flow by insect motion detection system: a model analysis

“…Much is known about the mechanisms of motion detection in insects and especially in flies at the level of neural circuits due to great methodological advances during recent years, (e.g., Borst, 2009; Reiff et al, 2010; Maisak et al, 2013; Silies et al, 2013; Takemura et al, 2013; Hopp et al, 2014; Mauss et al, 2014; Meier et al, 2014; Strother et al, 2014). The overall performance of these circuits can be lumped together and has been explained for long by a computational model of local motion detection, the correlation-type elementary motion detector (EMD), which also formed the basis of our study (Reichardt, 1961; Borst and Egelhaaf, 1989, 1993; Egelhaaf and Borst, 1993).…”

Fine and distributed subcellular retinotopy of excitatory inputs to the dendritic tree of a collision-detecting neuron

“…They have been widely studied on a population level in different species, for example, in the mammalian primary visual cortex (Adams and Horton 2003;Gias et al 2005;Schuett et al 2002), the auditory system of barn owls (Knudsen and Konishi 1978), and the electrosensory system of weakly electric fish (for review see Krahe and Maler 2014). At the subcellular level, studies using calcium imaging in neurons of the mammalian retina, the vertebrate optic tectum, and the insect visual system showed evidence of topographic dendritic input organization (Bollmann and Engert 2009;Euler et al 2002;Hopp et al 2014;Spalthoff et al 2010). However, how the morphological structure of dendrites and the specifics of topographically organized synaptic inputs influence synaptic integration and dendritic computation remains largely unknown.…”