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Adaptation and Temporal Decorrelation by Single Neurons in the Primary Visual Cortex

¹Volen Center for Complex Systems, Brandeis University, Waltham, Massachusetts 02454; ²Instituto de Neurociencias, Universidad Miguel Hernandez-Consejo Superior de Investigaciones Cientificas, San Juan de Alicante, Spain; and ³Department of Neurobiology, Yale University School of Medicine, New Haven, Connecticut 06510

Submitted 28 May 2002; accepted in final form 15 November 2002

Limiting redundancy in the real-world sensory inputs is of obvious benefit for efficient neural coding, but little is known about how this may be accomplished by biophysical neural mechanisms. One possible cellular mechanism is through adaptation to relatively constant inputs. Recent investigations in primary visual (V1) cortical neurons have demonstrated that adaptation to prolonged changes in stimulus contrast is mediated in part through intrinsic ionic currents, a Ca²⁺-activated K⁺ current (I_KCa) and especially a Na⁺-activated K⁺ current (I_KNa). The present study was designed to test the hypothesis that the activation of adaptation ionic currents may provide a cellular mechanism for temporal decorrelation in V1. A conductance-based neuron model was simulated, which included an I_KCa and an I_KNa. We show that the model neuron reproduces the adaptive behavior of V1 neurons in response to high contrast inputs. When the stimulus is stochastic with 1/f ² or 1/f-type temporal correlations, these autocorrelations are greatly reduced in the output spike train of the model neuron. The I_KCa is effective at reducing positive temporal correlations at approximately 100-ms time scale, while a slower adaptation mediated by I_KNa is effective in reducing temporal correlations over the range of 1–20 s. Intracellular injection of stochastic currents into layer 2/3 and 4 (pyramidal and stellate) neurons in ferret primary visual cortical slices revealed neuronal responses that exhibited temporal decorrelation in similarity with the model. Enhancing the slow afterhyperpolarization resulted in a strengthening of the decorrelation effect. These results demonstrate the intrinsic membrane properties of neocortical neurons provide a mechanism for decorrelation of sensory inputs.

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