Shifted encoding strategy in retinal luminance adaptation: from firing rate to neural correlation

Abstract

Neuronal responses to prolonged stimulation attenuate over time. Here, we ask a fundamental question: is adaptation a simple process for the neural system during which sustained input is ignored, or is it actually part of a strategy for the neural system to adjust its encoding properties dynamically? After simultaneously recording the activities of a group of bullfrog's retinal ganglion cells (dimming detectors) in response to sustained dimming stimulation, we applied a combination of information analysis approaches to explore the time-dependent nature of information encoding during the adaptation. We found that at the early stage of the adaptation, the stimulus information was mainly encoded in firing rates, whereas at the late stage of the adaptation, it was more encoded in neural correlations. Such a transition in encoding properties is not a simple consequence of the attenuation of neuronal firing rates, but rather involves an active change in the neural correlation strengths, suggesting that it is a strategy adopted by the neural system for functional purposes. Our results reveal that in encoding a prolonged stimulation, the neural system may utilize concerted, but less active, firings of neurons to encode information.retinal ganglion cell; luminance adaptation; information coding; neural correlation; discrimination ADAPTATION REFERS TO A GENERAL phenomenon in which a neural system adjusts its response property according to the statistics of external inputs (Kohn 2007;Wark et al. 2007). It has been widely suggested that adaptation underlies the strategy for a neural system to utilize its resource efficiently to encode stimulus information (Fairhall et al. 2001;Gutnisky and Dragoi 2008;Lesica et al. 2007;Maravall et al. 2007). For instance, it was found that the tuning functions of sensory neurons are optimized to match the variance of inputs in a natural environment, so that high encoding accuracy for the whole range of stimuli is achieved (Laughlin 1981). In practice, adaptation can also occur very rapidly in response to sudden changes in the input statistics, so that the stimulus information is transmitted with high fidelity (Fairhall et al. 2001;Sharpee et al. 2006). A recent experimental work reported that in addition to enhancing information representation, adaptation can regulate information content transmitted in the sensory pathway (Wang et al. 2010). Thus, to fully understand how the brain processes stimulus information in a natural dynamical environment, it is critical to unveil the computational roles associated with adaptation.Luminance adaptation, in which a neural system is exposed to a sustained stimulation with constant luminance, is a fundamental visual adaptation process whose biophysical mechanisms and potential computational roles have been intensively studied (Wark et al. 2007). However, the detailed time course as to how the stimulus information is encoded dynamically in the varying neural responses during adaptation remains largely unresolved (Kastner and Baccus 2011). In luminance ad...

Nonlinear dendritic integration of electrical and chemical synaptic inputs drives fine-scale correlations

“…Although this property appears to be consistent with findings for other gap junction–coupled neurons 39,40 , it sharply contrasts with synchrony generated by common input measured in other parts of the brain, where output correlations are found to increase with spike rate 36,37 . Correlations driven by common input are generally found to be weak at low spike rates because they are masked by the spike threshold and therefore only become evident at higher activity levels 36,37 .…”

Effects of dopamine on response properties of ON-OFF RGCs in encoding stimulus durations

“…Furthermore, ON and OFF RGCs have different excitatory and inhibitory synaptic inputs, which results in different spike time and spike count variability in these cells (Uzzell and Chichilnisky, 2004; Murphy and Rieke, 2006). These differences in the neural network between retinal ON and OFF pathways may induce different encoding strategies in neuronal ON and OFF responses (Zaghloul et al, 2003; Masland, 2012; Harris and Mrsic-Flogel, 2013; Xiao et al, 2013). …”

“…Experiments were performed on isolated bullfrog retinas at room temperature (22–26°C) (Jing et al, 2010; Xiao et al, 2013, 2014). Bullfrogs were dark adapted for about 30 min prior to experiments.…”

“…Before application of stimulation protocols, full-field sustained dim white light (38.9 nW/cm 2 ) was given for 30 s to adjust the RGCs' sensitivity to similar levels (Jing et al, 2010; Xiao et al, 2013). …”

Characterization of Predictive Behavior of a Retina by Mutual Information

“…A piece of retinal tissue (~2 × 2 mm 2 ) is fixed on the MEA by a permeable membrane and perfused with oxygenated Ringer's solution (NaCl 100.0, KCl 2.5, MgCl 2 1.6, CaCl 2 1.0, NaHCO 3 18.0, Glucose 10.0 mM). Each retina preparation can last for 6–8 h for experiments (Ishikane et al, 2005; Xiao et al, 2013). Retinal activities are recorded by MEA with 200 μm inter-electrode distance and 10 μm electrode diameter (MEA60-200-10-PtBlack, Qwane Bioscience).…”