Functional-pathway-dominant contrast adaptation and sensitization in mouse retinal ganglion cells

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RESEARCH ARTICLE

Functional-pathway-dominant contrast adaptation and sensitization in mouse retinal ganglion cells Min Dai1 • Pei-Ji Liang1 Received: 2 March 2020 / Revised: 3 September 2020 / Accepted: 14 September 2020 Ó Springer Nature B.V. 2020

Abstract Retinal ganglion cells (RGCs) reduce their light sensitivity during persistent high-contrast stimulation to prevent saturation to strong inputs and improve coding efficiency. This process is known as contrast adaptation. However, contrast adaptation also reduces RGCs’ light response to weak inputs. On the other hand, some RGCs undergo contrast sensitization, and these RGCs respond to weak inputs following high contrast stimulation. In the present study, multi-electrode recordings were conducted on isolated mouse retinas under full-field visual stimulation with different contrast levels. Adaptation and sensitization were mainly observed in OFF and ON pathways, respectively. The results of linear–nonlinear analysis and stimulus reconstruction revealed that both the light sensitivity and encoded information were changed in opposite directions in adaptation and sensitization processes. Our work suggests that contrast adaptation and sensitization are two opposite dynamic processes. In mouse retina, OFF RGCs utilize adaptation to increase the discrimination of strong OFF inputs. On the other hand, ON RGCs use sensitization to increase the sensitivity to weak ON inputs. This functional differentiation might be meaningful for the mouse’s survival as it lives in environments in which strong OFF stimuli often indicate potential predators while weak ON stimuli are usually related to movement and might be important for predation. Keywords Retinal ganglion cells  Multi-electrode recording  Linear–nonlinear model  Stimulus reconstruction  Visual information

Introduction Luminance in the natural environment changes within a 1011-fold range, from about 10-6 cd/m2 in darkness to 105 cd/m2 in full sunlight (Reinagel 2001). However, neuronal activity only covers a narrow operating range of no more than 102-fold (Demb and Singer 2015). Therefore, the visual neural system must continuously adjust its responsiveness to match the dynamic input. To achieve this, a number of strategies are involved, which includes visual adaptation to ambient luminance and contrast. It has been well observed that neurons fire with relatively high rates at the onset of high-contrast stimulation and activity gradually adapts to persistent stimulation, preventing saturation to strong inputs (Demb 2008) thus increasing coding & Pei-Ji Liang [email protected] 1

School of Biomedical Engineering, Shanghai Jiao Tong University, 800 Dong-Chuan Road, Shanghai 200240, China

efficiency (Durant et al. 2007; Jin et al. 2005). However, this adaptation also makes neurons less sensitive to weak inputs (Baccus and Meister 2002; Brown and Masland 2001; Manookin and Demb 2006). Indeed it has been reported that in some retinal neurons, another dynamic process characteri