Synaptic and intrinsic mechanisms underlying development of cortical direction selectivity

Modifications of synaptic inputs and cell-intrinsic properties both contribute to neuronal plasticity and development. To better understand these mechanisms, we undertook an intracellular analysis of the development of direction selectivity in the ferret visual cortex, which occurs rapidly over a few days after eye opening. We found strong evidence of developmental changes in linear spatiotemporal receptive fields of simple cells, implying alterations in circuit inputs. Further, this receptive field plasticity was accompanied by increases in near-spike-threshold excitability and input-output gain that resulted in dramatically increased spiking responses in the experienced state. Increases in subthreshold membrane responses induced by the receptive field plasticity and the increased input-output spiking gain were both necessary to explain the elevated firing rates in experienced ferrets. These results demonstrate that cortical direction selectivity develops through a combination of plasticity in inputs and in cell-intrinsic properties.

Synaptic and intrinsic mechanisms underlying development of cortical direction selectivity

Some neural circuits are constructed through an overproduction of initial connections followed by activity-dependent refinement. Under this paradigm, functional receptive fields would be expected to be narrowed from a diffuse immature condition to a sharper mature condition. Alternatively, neural activity might lead to formation of new connections, leading to expansion of an initially compact receptive field. In the simple cells of the ferret visual cortex undergoing developmental enhancement of direction selectivity, we found evidence for a mixed mechanism: an expansion of the spatiotemporal receptive fields along the temporal dimension combined with a narrowing in space-time through a marked loss of inputs with certain space-time selectivities. Further, the resulting increase in subthreshold direction selectivity was accompanied by increases in near-spike-threshold excitability and input-output gain that resulted in dramatically increased spiking responses. Increases in subthreshold membrane responses and the increased input-output spiking gain were both necessary to explain firing rates in experienced ferrets. These results demonstrate that cortical direction selectivity develops through a combination of plasticity in synaptic and cell-intrinsic properties.

Ambient illumination switches contrast preference of specific retinal processing streams

Contrast, a fundamental feature of visual scenes, is encoded in a distributed manner by ∼20 retinal ganglion cell (RGC) types, which stream visual information to the brain. RGC types respond preferentially to positive (ONpref) or negative (OFFpref) contrast and differ in their sensitivity to preferred contrast and responsiveness to nonpreferred stimuli. Vision operates over an enormous range of mean light levels. The influence of ambient illumination on contrast encoding across RGC types is not well understood. Here, we used large-scale multielectrode array recordings to characterize responses of mouse RGCs under lighting conditions spanning five orders in brightness magnitude. We identify three functional RGC types that switch contrast preference in a luminance-dependent manner (Sw1-, Sw2-, and Sw3-RGCs). As ambient illumination increases, Sw1- and Sw2-RGCs shift from ONpref to OFFpref and Sw3-RGCs from OFFpref to ONpref. In all cases, transitions in contrast preference are reversible and track light levels. By mapping spatiotemporal receptive fields at different mean light levels, we find that changes in input from ON and OFF pathways in receptive field centers underlie shifts in contrast preference. Sw2-RGCs exhibit direction-selective responses to motion stimuli. Despite changing contrast preference, direction selectivity of Sw2-RGCs and other RGCs as well as orientation-selective responses of RGCs remain stable across light levels.

Applicability of White-Noise Techniques to Analyzing Motion Responses

Motion processing in visual neurons is often understood in terms of how they integrate light stimuli in space and time. These integrative properties, known as the spatiotemporal receptive fields (STRFs), are sometimes obtained using white-noise techniques where a continuous random contrast sequence is delivered to each spatial location within the cell's field of view. In contrast, motion stimuli such as moving bars are usually presented intermittently. Here we compare the STRF prediction of a neuron's response to a moving bar with the measured response in second-order interneurons (L-neurons) of dragonfly ocelli (simple eyes). These low-latency neurons transmit sudden changes in intensity and motion information to mediate flight and gaze stabilization reflexes. A white-noise analysis is made of the responses of L-neurons to random bar stimuli delivered either every frame (densely) or intermittently (sparsely) with a temporal sequence matched to the bar motion stimulus. Linear STRFs estimated using the sparse stimulus were significantly better at predicting the responses to moving bars than the STRFs estimated using a traditional dense white-noise stimulus, even when second-order nonlinear terms were added. Our results strongly suggest that visual adaptation significantly modifies the linear STRF properties of L-neurons in dragonfly ocelli during dense white-noise stimulation. We discuss the ability to predict the responses of visual neurons to arbitrary stimuli based on white-noise analysis. We also discuss the likely functional advantages that adaptive receptive field structures provide for stabilizing attitude during hover and forward flight in dragonflies.