Subcellular Topography of Visually Driven Dendritic Activity in the Vertebrate Visual System

Abstract

SUMMARY Neural pathways projecting from sensory organs to higher brain centers form topographic maps in which neighbor relationships are preserved from a sending to a receiving neural population. Sensory input can generate compartmentalized electrical and biochemical activity in the dendrites of a receiving neuron. Here, we show that in the developing retinotectal projection of young Xenopus tadpoles, visually driven Ca2+ signals are topographically organized at the subcellular, dendritic scale. Functional in vivo two-photon Ca2+ imaging revealed that the sensitivity of dendritic Ca2+ signals to stimulus location in visual space is correlated with their anatomical position within the dendritic tree of individual neurons. This topographic distribution was dependent on NMDAR activation, whereas global Ca2+ signals were mediated by Ca2+ influx through dendritic, voltage-dependent Ca2+ channels. These findings suggest a framework for plasticity models that invoke local dendritic Ca2+ signaling in the elaboration of neural connectivity and dendrite-specific information storage.

Subcellular mapping of dendritic activity in optic flow processing neurons

“…In the tectum of Xenopus larvae, a topographic bias of the dendritic response to different elevations of a flicker stimulus has been reported [8]. In the lobula giant movement detector neuron in the visual system of the locust, a retinotopic mapping has been rigorously established down to the level of single ommatidia [11].…”

“…Few studies have investigated the subcellular distribution of sensory inputs: In the mammalian visual [4], vibrissal [5], as well as auditory [6] cortex, inputs tuned to different ranges of a specific stimulus parameter are scattered across the dendrite, lacking any particular spatial organization. In contrast, neurons in the mammalian retina [7], the vertebrate tectum [8], and the insect visual system [9] show evidence of a topographic input organization. in a quantitative way and accounts for their observations in remarkable detail.…”

Wnt/PCP proteins regulate stereotyped axon branch extension inDrosophila

“…Conversely, dendrite branches collate disparate nerve inputs and their integrative function is key to signal processing. Branched structures along a nerve segment also have physiological properties that propagate, disperse and spatially represent nerve signals (Baccus et al, 2000;Huguenard, 2000;Bollmann and Engert, 2009;Foust et al, 2010). How branched structures form is unclear.…”

The horizontal brain slice preparation: a novel approach for visualizing and recording from all layers of the tadpole tectum

“…The mechanism(s) underlying how different sets of inputs are consistently guided to specific regions of the dendrite, however, is (are) not completely clear. It has been suggested that synchronous activity of all of the axons associated with specific sensory input could account for "like" axons converging onto a specific focused region of the dendrite (Bollmann and Engert 2009). Consistent with this, in the tadpole tectum, the RGC and mechanosensory inputs arrive simultaneously (Hiramoto and Cline 2009), suggesting the possibility that activity-dependent competition between the different sensory inputs underlies their segregation.…”

“…In addition to the segregation of visual RGC and mechanosensory (HB) inputs in the tadpole tectum, individual axons that constitute the RGC input are further organized within the distal region of dendrite according to the position of the RGC in the eye: RGCs of the dorsal region of the eye project to the more medial portion of the distal dendrites, whereas RGCs of the ventral region of the eye project to the lateral portion (Bollmann and Engert 2009). Similarly, in zebrafish, it has been shown that the spatial pattern of visual inputs is arranged in tectal space according to the direction selectivity of the individual axons (Gabriel et al 2012).…”