The Impact of Ecological Niche on Adaptive Flexibility of Sensory Circuitry

Abstract

Evolution and development are interdependent, particularly with regard to the construction of the nervous system and its position as the machine that produces behavior. On the one hand, the processes directing development and plasticity of the brain provide avenues through which natural selection can sculpt neural cell fate and connectivity, and on the other hand, they are themselves subject to selection pressure. For example, mutations that produce heritable perturbations in neuronal birth and death rates, transcription factor expression, or availability of axon guidance factors within sensory pathways can markedly affect the development of form and thus the function of stimulus decoding circuitry. This evolvability of flexible circuits makes them more adaptable to environmental variation. Although there is general agreement on this point, whether the sensitivity of circuits to environmental influence and the mechanisms underlying development and plasticity of sensory pathways are similar across species from different ecological niches has received almost no attention. Neural circuits are generally more sensitive to environmental influences during an early critical period, but not all niches afford the same access to stimuli in early life. Furthermore, depending on predictability of the habitat and ecological niche, sensory coding circuits might be more susceptible to sensory experience in some species than in others. Despite decades of work on understanding the mechanisms underlying critical period plasticity, the importance of ecological niche in visual pathway development has received little attention. Here, I will explore the relationship between critical period plasticity and ecological niche in mammalian sensory pathways.

Phenotypic plasticity in Periplaneta americana photoreceptors

“…Environmental stimuli contribute to the proper development and maintenance of sensory receptors and their downstream neural circuits. In visual systems, the effects of such stimulation, or its lack, can range from a failure to establish proper synaptic connections during ontogenesis (Hubel and Wiesel, 1970; Hubel et al, 1977; Jiang et al, 2009) to various forms of synaptic plasticity (Berry and Nedivi, 2016; Pallas, 2017). For peripheral visual systems, numerous short- and long-term activity–dependent modifications have been described over different time scales at both the cellular and network levels in photoreceptors and higher-order visual neurons (Brann and Cohen, 1987; Sokolov et al, 2002; Wagner and Kröger, 2005; Calvert et al, 2006).…”

“…Studies of plasticity in invertebrate visual systems have examined developmental changes at the first visual synapse, connections between neurons in the higher-order visual centers (Hertel, 1983; Meinertzhagen, 1989; Barth et al, 1997; Pallas, 2017), short-term light adaptations in the retina (Laughlin, 1989), and illumination-dependent changes at the molecular level in photoreceptors (Bähner et al, 2002; Cronin et al, 2006; Frechter and Minke, 2006). However, little is known about long-term functional adaptations in microvillar photoreceptors.…”

Multiple Postsynaptic Protein Levels in Adult Superior Colliculus Are Unaffected by Dark Rearing from Birth

“…Once these critical periods have closed, plasticity is often limited or even prevented, thus protecting refined circuits from destabilization (Hensch and Quinlan, 2018;Hubel and Wiesel, 1970;Hübener and Bonhoeffer, 2014;Pallas, 2017;Reh et al, 2020;Ribic, 2020;Takesian and Hensch, 2013). In some mammals, visual deprivation is reported to delay or prevent refinement, prolonging critical period plasticity (Cynader and Mitchell, 1980;Fagiolini et al, 1994;Lee and Nedivi, 2002;Mower, 1991;Mower et al, 1985;Nakadate et al, 2012).…”

“…In the visual pathway, although spontaneous retinal activity is important for initial pruning, it is historically thought that early visual experience is essential for attainment of refined connectivity patterns (Firth et al, 2005; Katz and Shatz, 1996; Maffei and Galli-Resta, 1990; Meister et al, 1991; Ruthazer and Cline, 2004; Wong et al, 1993). Once these critical periods have closed, plasticity is often limited or even prevented, thus protecting refined circuits from destabilization (Hensch and Quinlan, 2018; Hubel and Wiesel, 1970; Hübener and Bonhoeffer, 2014; Pallas, 2017; Reh et al, 2020; Ribic, 2020; Takesian and Hensch, 2013). In some mammals, visual deprivation is reported to delay or prevent refinement, prolonging critical period plasticity (Cynader and Mitchell, 1980; Fagiolini et al, 1994; Lee and Nedivi, 2002; Mower, 1991; Mower et al, 1985; Nakadate et al, 2012).…”

Postnatal Development of Visual Cortical Function in the Mammalian Brain

“…Collectively, these data suggest that differences exist in the type of experience or duration that differs among species, but even within a species among different response properties (Aboitiz et al, 2018). Nonetheless, little effort has been made to relate these differences to the behavioral ecology of a species, which is likely to play a major role in how visual experience differentially affects the refinement of neuronal response properties (Pallas, 2017).…”