Contrast sensitization [electronic resource] : function, theory, and mechanism of a novel retinal computation

Adaptation provides a ubiquitous strategy for neural circuits to encode their inputs using their limited dynamic range within the variety of sensory environments that they encounter. However, because of the inherent timescale necessary to optimize the response properties of a cell to its environment, any form of adaptive plasticity can cause a neuron to fail to encode the stimulus when the environment changes. Many ganglion cells, the output neurons of the retina, adapt so as to lower their sensitivity in an environment of high contrast, but if the contrast subsequently decreases the cell will fall below threshold and fail to signal. I have found a distinct form of plasticity within the retina that acts in coordination with the process of adaptation. Cells using this new form of plasticity elevate their sensitivity after a transition to low contrast. This process, called sensitization, occurs in retinas from multiple species. Multielectrode recordings from sensitizing and adapting cells indicate that both populations encode the same visual signals. The complementary action of the two populations helps the retina encode its input over a broader range of signals and environmental changes, with one population continuing to respond when the other fails. The threshold placement of these two cell types further enhances their coordination because sensitizing cells maintain lower thresholds, while adapting cells maintain higher thresholds. Using a theoretical model, I was able to show that this behavior maximized the amount of information that the two populations can provide about their input. I have further studied the spatiotemporal region that controlled the sensitivity of a cell--the adaptive field. Just as retinal circuitry uses excitation and inhibition to form biphasic center-surround receptive fields, the retina can also use adaptation and sensitization to form biphasic adaptive fields in both the spatial and temporal domains. Since visual statistics are correlated across time and space, center-surround biphasic receptive fields more efficiently encode the input by subtracting a prediction of the stimulus so as to just encode the deviation from that prediction. Biphasic adaptive fields appear to perform an opposite function, transmitting a prediction of the stimulus at the transition of a stimulus environment to weaker signals. This assists in the encoding of an uncertain environment by storing features of a predictable input. A model indicates that sensitization within the adaptive field can be produced by adapting inhibition, a form of plasticity whose function was previously unknown. Using pharmacology, I confirmed this prediction, showing that GABAergic inhibition is necessary for sensitization. Using simultaneous intracellular recording from inhibitory amacrine cells and multielectrode recording from ganglion cells, I show that transmission from a single amacrine cell is sucient to cause sensitization. Using a novel approach to analyze a circuit, I quantitatively describe the changes in amacrine cell transmission that underlie sensitization thus elucidating how the retina performs this sophisticated computation.

Advisor: Baccus Stephen A. primary advisor. Thesis advisor
Baylor Denis
Tsien R. W. (Richard W.) advisor. Thesis advisor
Wandell Brian A. advisor. Thesis advisor