The Role of Dendrites in the Organization of Functional Neural Circuits for Motion Detection in the Retina
Retinal ganglion cells (RGCs) represent the output computations of the visual world. In the mouse, they represent >30 parallel channels of visual processing, encoding both image-forming and non-image forming features. The dendrites of RGCs are considered essential in ensuring that the downstream visual system receives a full depiction of the sampled visual field. Different retinal ganglion cell types have evolved a multitude of dendritic arbor architectures that allow them to efficiently encode the spatial and temporal features of the visual scene that they are tuned to. Despite this fundamental role of dendritic morphology, there are relatively few studies that directly test whether different dendritic morphologies lead to variations in the wiring and resulting computations within a neural circuit.
This main body of this work has aimed to address this question in a well-defined neural circuit in the retina that is responsible for our ability to detect the direction an object moves in the visual world. Direction selectivity is a neural computation where a directionally selective retinal ganglion cell (DSGC), one of the output neurons of the retina whose axons comprise the optic nerve, fire more action potentials in response to motion in one direction, versus motion in the opposite direction. Multiple presynaptic mechanisms involving the specific wiring of excitatory and inhibitory inputs onto DSGC dendrites have been postulated to contribute to the direction selectivity computation. Additionally, postsynaptic computations within the DSGC dendrites have been postulated to sharpen their directional tuning
Here, we explore how DSGC dendrites contribute to both the presynaptic organization of excitatory and inhibitory inputs, and the postsynaptic contribution to directional tuning. First, we show that visual experience influences the dendritic orientation in a population of asymmetric ventral preferring DSGCs (vDSGCs) whose dendrites point ventrally. By comparing the tuning of normally versus dark-reared vDSGCs, we find that their tuning to ventral motion is preserved regardless of their dendritic orientation. This is due to the persistence of asymmetric wiring of inhibition in dark-reared vDSGCs. However, we find that the ventral orientation of vDSGC dendrites is necessary for their postsynaptic directional computation, which occurs in the absence of inhibitory input. Hence, in vDSGCs, dendritic morphology dictates postsynaptic but not presynaptic mechanisms for directional computation.
Second, we show that dendritic morphology, across two distinct populations of DSGCs, does not determine the organization of presynaptic inputs. By comparing the excitatory and inhibitory receptive fields across two morphologically distinct DSGC subtypes, we find that although asymmetric DSGCs exhibit greater tuning of their inhibitory input in response to a moving stimulus, compared to symmetric DSGCs, the synaptic organization of excitation relative to inhibition is comparable across cell types. Hence, DSGC dendritic morphology does not dictate the organization of excitatory and inhibitory synaptic inputs relative to each other.