Synaptic and intrinsic mechanisms underlying development of cortical direction selectivity

Abstract

In the primary visual cortex (V1) of carnivores and primates, early visual experience shapes the development of functional properties such as selectivity for direction of motion. However, it remains unclear which aspects of the cortical circuitry -synaptic and/or cellintrinsic -are molded by the visual activity, and how. Therefore, we performed in vivo intracellular recordings from V1 simple cells in visually naive and experienced ferrets, and computed their membrane potential (Vm) spatiotemporal receptive fields and Vm-to-spike input-output transfer functions. Comparison across the two developmental stages revealed marked reorganization of inputs and a sharp enhancement of input-output gain in the experienced state, leading to prodigious amplification of direction selectivity at the spiking level. Simultaneously, we detected a lowering of spike thresholds and an intensification of gamma-band Vm oscillations, which might explain the enhancement of spiking. Thus, direction selectivity develops through combined processes of synaptic re-wiring and maturation of cell-intrinsic properties.

Balanced Enhancements of Synaptic Excitation and Inhibition Underlie Developmental Maturation of Receptive Fields in the Mouse Visual Cortex

“…The suppression of high spontaneous activity is consistent with the notion of an increasing inhibitory tone during the post-eye-opening development (Chattopadhyaya, 2004;Morales et al, 2002). The developmental trends of decreases in spontaneous firing rates and increases in visually evoked responses generally agree with the results of several previous studies (Hoy and Niell, 2015;Li et al, 2012;Roy et al, 2020), although they have not reached statistical significance in layer 4 in one study (Hoy and Niell, 2015). As shown in Fig.…”

“…Nevertheless, we do not exclude the possibility that changes of other membrane properties, e.g. lowering of spike threshold (Roy et al, 2020), can further contribute to the increased salience of visually evoked activity and detectability of RFs.…”

“…High-quality visual function is progressively established during development, which depends on the concurrence of correct initial neural wiring and appropriately patterned sensory inputs (Cang and Feldheim, 2013;Espinosa and Stryker, 2012;Hooks and Chen, 2020;White and Fitzpatrick, 2007). This experience-dependent visual development is most prominent at the cortical level and peaks at the critical period (Berardi et al, 2000;Hensch, 2005;Trachtenberg, 2015), during which various important visual functionalities, including ocular dominance (Fagiolini et al, 1994;Hofer et al, 2006;Shatz and Stryker, 1978;Stephany et al, 2018), binocularity (Jenks and Shepherd, 2020;Tian et al, 2020), orientation selectivity (Chapman and Stryker, 1993;Hoy and Niell, 2015;Li et al, 2012;Moore and Freeman, 2012;White et al, 2001), direction selectivity (Clemens et al, 2012;Hoy and Niell, 2015;Li et al, 2006Li et al, , 2008Rochefort et al, 2011;Roy et al, 2020;Smith et al, 2015) and binocular matching (Chang et al, 2020;Wang et al, 2010;Wang et al, 2015), are established, or refined and strengthened. Sensory deprivation such as dark rearing (DR) can affect the critical period and normal development of visual functionalities (Fagiolini et al, 1994;Gianfranceschi et al, 2003;Hubel and Wiesel, 1970;Jenks and Shepherd, 2020;Kang et al, 2013;Ko et al, 2014;Li et al, 2012;…”

“…However, research on the developmental evolution of RF structure in the visual cortex has remained limited (Braastad and Heggelund, 1985;Hoy and Niell, 2015;Ko et al, 2013;Roy et al, 2020;Sarnaik et al, 2014;Smith et al, 2017). While a recent study in the developing mouse primary visual cortex (V1) has reported a slight shift towards more RF subunits and more elongated RFs over development (Hoy and Niell, 2015), how the synaptic input architecture underlying the spatial RF evolves during normal development and whether this process can be affected by sensory deprivation remains elusive.…”