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The cellular and molecular basis of direction selectivity of A?-LTMRs.

ABSTRACT: The perception of touch, including the direction of stimulus movement across the skin, begins with activation of low-threshold mechanosensory neurons (LTMRs) that innervate the skin. Here, we show that murine A?-LTMRs are preferentially tuned to deflection of body hairs in the caudal-to-rostral direction. This tuning property is explained by the finding that A?-LTMR lanceolate endings around hair follicles are polarized; they are concentrated on the caudal (downward) side of each hair follicle. The neurotrophic factor BDNF is synthesized in epithelial cells on the caudal, but not rostral, side of hair follicles, in close proximity to A?-LTMR lanceolate endings, which express TrkB. Moreover, ablation of BDNF in hair follicle epithelial cells disrupts polarization of A?-LTMR lanceolate endings and results in randomization of A?-LTMR responses to hair deflection. Thus, BDNF-TrkB signaling directs polarization of A?-LTMR lanceolate endings, which underlies direction-selective responsiveness of A?-LTMRs to hair deflection.

SUBMITTER: Rutlin M

PROVIDER: S-EPMC4297767 | biostudies-literature | 2014 Dec

REPOSITORIES: biostudies-literature

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The cellular and molecular basis of direction selectivity of Aδ-LTMRs.

Rutlin Michael M Ho Cheng-Ying CY Abraira Victoria E VE Cassidy Colleen C Bai Ling L Woodbury C Jeffery CJ Ginty David D DD

Cell 20141201 7

The perception of touch, including the direction of stimulus movement across the skin, begins with activation of low-threshold mechanosensory neurons (LTMRs) that innervate the skin. Here, we show that murine Aδ-LTMRs are preferentially tuned to deflection of body hairs in the caudal-to-rostral direction. This tuning property is explained by the finding that Aδ-LTMR lanceolate endings around hair follicles are polarized; they are concentrated on the caudal (downward) side of each hair follicle. ...[more]

PMID: 25525881

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Project description:The discrimination of the direction of movement of sensory images is critical to the control of many animal behaviors. We propose a parsimonious model of motion processing that generates direction selective responses using short-term synaptic depression and can reproduce salient features of direction selectivity found in a population of neurons in the midbrain of the weakly electric fish Eigenmannia virescens. The model achieves direction selectivity with an elementary Reichardt motion detector: information from spatially separated receptive fields converges onto a neuron via dynamically different pathways. In the model, these differences arise from convergence of information through distinct synapses that either exhibit or do not exhibit short-term synaptic depression--short-term depression produces phase-advances relative to nondepressing synapses. Short-term depression is modeled using two state-variables, a fast process with a time constant on the order of tens to hundreds of milliseconds, and a slow process with a time constant on the order of seconds to tens of seconds. These processes correspond to naturally occurring time constants observed at synapses that exhibit short-term depression. Inclusion of the fast process is sufficient for the generation of temporal disparities that are necessary for direction selectivity in the elementary Reichardt circuit. The addition of the slow process can enhance direction selectivity over time for stimuli that are sustained for periods of seconds or more. Transient (i.e., short-duration) stimuli do not evoke the slow process and therefore do not elicit enhanced direction selectivity. The addition of a sustained global, synchronous oscillation in the gamma frequency range can, however, drive the slow process and enhance direction selectivity to transient stimuli. This enhancement effect does not, however, occur for all combinations of model parameters. The ratio of depressing and nondepressing synapses determines the effects of the addition of the global synchronous oscillation on direction selectivity. These ingredients, short-term depression, spatial convergence, and gamma-band oscillations, are ubiquitous in sensory systems and may be used in Reichardt-style circuits for the generation and enhancement of a variety of biologically relevant spatiotemporal computations.

Dataset Information

The cellular and molecular basis of direction selectivity of A?-LTMRs.

Publications

The cellular and molecular basis of direction selectivity of Aδ-LTMRs.

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