The Wiring of Developing Sensory Circuits—From Patterned Spontaneous Activity to Synaptic Plasticity Mechanisms

Abstract

In order to accurately process incoming sensory stimuli, neurons must be organized into functional networks, with both genetic and environmental factors influencing the precise arrangement of connections between cells. Teasing apart the relative contributions of molecular guidance cues, spontaneous activity and visual experience during this maturation is on-going. During development of the sensory system, the first, rough organization of connections is created by molecular factors. These connections are then modulated by the intrinsically generated activity of neurons, even before the senses have become operational. Spontaneous waves of depolarizations sweep across the nervous system, placing them in a prime position to strengthen correct connections and weaken others, shaping synapses into a useful network. A large body of work now support the idea that, rather than being a mere side-effect of the system, spontaneous activity actually contains information which readies the nervous system so that, as soon as the senses become active, sensory information can be utilized by the animal. An example is the neonatal mouse. As soon as the eyelids first open, neurons in the cortex respond to visual information without the animal having previously encountered structured sensory input (Cang et al., 2005b; Rochefort et al., 2011; Zhang et al., 2012; Ko et al., 2013). In vivo imaging techniques have advanced considerably, allowing observation of the natural activity in the brain of living animals down to the level of the individual synapse. New (opto)genetic methods make it possible to subtly modulate the spatio-temporal properties of activity, aiding our understanding of how these characteristics relate to the function of spontaneous activity. Such experiments have had a huge impact on our knowledge by permitting direct testing of ideas about the plasticity mechanisms at play in the intact system, opening up a provocative range of fresh questions. Here, we intend to outline the most recent descriptions of spontaneous activity patterns in rodent developing sensory areas, as well as the inferences we can make about the information content of those activity patterns and ideas about the plasticity rules that allow this activity to shape the young brain.

Topographic map refinement and synaptic strengthening of a sound localization circuit require spontaneous peripheral activity

“…The elegant Clause study provides strong evidence that the spontaneous activity pattern carries information for proper MNTB–LSO circuit refinement. Moreover, our study is in line with results from other developing neural circuits in the neocortex, the spinal cord, the hippocampus and the cerebellum (Blankenship & Feller, ; Leighton & Lohmann, ; Luhmann et al . ).…”

“…The excitation occurs in a conserved temporal pattern (Tritsch et al 2010), implying that IHCs generate pace-making activity. Spatially restricted and synchronous spontaneous activity provided by IHCs may be an instructive cue for the development of precise topographic maps in the auditory system (Friauf & Lohmann, 1999;Kandler et al 2009;Leighton & Lohmann, 2016). Auditory synaptopathy in Otof deaf5/deaf5 mice likely drastically reduces, or even abolishes, spontaneous activity and hence activity propagation from the periphery to central targets.…”

Actin remodeling, the synaptic tag and the maintenance of synaptic plasticity

“…Interestingly, the charge of such dendritic spike is much higher than the linear sum of all the activated synapses, spreading much more efficiently to the soma and increasing the probability of somatic action‐potential generation . Like in many aspects in nature the “The Whole is Greater than the Sum of its Parts.” Additionally, these non‐linear dendritic integration events can be modulated by local plasticity mechanisms, again supporting the model that dendritic compartments operate as an integrative and discrete computational unit …”

“…Additionally, these non-linear dendritic integration events can be modulated by local plasticity mechanisms, again supporting the model that dendritic compartments operate as an integrative and discrete computational unit. 57,58 This model of dendritic compartments also holds if one looks at biochemical compartments, either local calcium signals or PRPs activation. While activation of individual spines in hippocampal pyramidal cells has been shown to give rise to spine-restricted calcium signals, following dendritic spikes, activation of glutamate and voltage-gated calcium channels leads to a calcium rise that spread in the dendritic branch.…”

Two dimensional model of learning in spiking neural networks with homeostasis and reward

“…Якщо врахувати гіпотезу, що спонтанна активність, симульована через розподіл Пуассона, дійсно має просторово часові кореляції [18], які відпові-дають попередньо навченим стимулам, тоді гомеостаз відновиться швидше і помітно не зменшиться період неактивності.…”