Role of emergent neural activity in visual map development

Abstract

The initial structural and functional development of visual circuits in reptiles, birds, and mammals happens independent of sensory experience. After eye opening, visual experience further refines and elaborates circuits that are critical for normal visual function. Innate genetic programs that code for gradients of molecules provide gross positional information for developing nerve cells, yet much of the cytoarchitectural complexity and synaptogenesis of neurons depends on calcium influx, neurotransmitter release, and neural activity before the onset of vision. In fact, specific spatiotemporal patterns of neural activity, or 'retinal waves', emerge amidst the development of the earliest connections made between excitable cells in the developing eye. These patterns of spontaneous activity, which have been observed in all amniote retinae examined to date, may be an evolved adaptation for species with long gestational periods before the onset of functional vision, imparting an informational robustness and redundancy to guide development of visual maps across the nervous system. Recent experiments indicate that retinal waves play a crucial role in the development of interconnections between different parts of the visual system, suggesting that these spontaneous patterns serve as a template-matching mechanism to prepare higher-order visually associative circuits for the onset of visuomotor learning and behavior. Key questions for future studies include determining the exact sources and nature of spontaneous activity during development, characterizing the interactions between neural activity and transcriptional gene regulation, and understanding the extent of circuit connectivity governed by retinal waves within and between sensory-motor systems.

Figure 1

Retinal waves drive patterned activity in the developing visual system. Image shows summed population activity after ablation of retinal input from the left eye in P6 mouse. Calcium signals are color coded by time of retinal wave front propagation in the SC-L. Notice the lack of activity in SC-R and V1-R. Data are based on unpublished results from [26], and consist of merged fields of view from two subsequent recordings (80 s total; SC-L+SC-R with V1-L or V1-R), overlaid on an Allen Developing Mouse Brain Atlas P4 reference illustration.

Figure 2

Efferent connectivity from mouse visual cortex. Reference image (top left) adapted from Allen Mouse Brain Atlas. Axonal projections (right and bottom panels) are color coded by target structure and were rendered using two primary visual cortex injection datasets (black dots indicate injection location) available from the Allen Mouse Brain Connectivity Atlas.