Repetitive adaptation induces plasticity of spatial frequency tuning in cat primary visual cortex

Abstract

Sensory neurons display transient changes in their response properties following prolonged exposure to an appropriate stimulus (adaptation). In adult cat primary visual cortex, spatial frequency-selective neurons shift their preferred spatial frequency (SF) after being adapted to a non-preferred SF. In anesthetized cats prepared for electrophysiological recordings in the visual cortex, we applied a non-preferred spatial frequency for two successive periods of adaptation (a recovery and interval of ∼90 min separated both phases of adaptation) in order to determine if a first adaptation retained an influence on a second adaptation. The first application of a non-preferred SF shifted the tuning curve of the cell mainly in the direction of the imposed SF. The results showed that attractive shifts occurred more frequently (68%) than repulsive (12%) changes in cortical cells. The increase of responsivity was band-limited and occurred around the imposed SF, while flanked responses remained unmodified in all conditions. After a recovery period allowing neurons to restore their original SF tuning curves, we carried out a second adaptation which produced four major results: (1) a higher proportion of repulsive shifts (31%) compared to attractive shifts (49%), (2) an increase of the magnitude of the attractive shifts, (3) an additional enhancement of the evoked firing rate for the newly acquired SF, and (4) for the acquired SF the variability coefficient decreased following the second adaptation. The supplementary response changes suggest that neurons in area 17 keep a “memory” trace of the previous stimulus properties. It also highlights the dynamic nature of basic neuronal properties in adult cortex since repeated adaptations modified both the spatial frequency tuning selectivity and the response strength to the preferred spatial frequency. These enhanced neuronal responses suggest that the range of adaptation-induced plasticity available to the visual system is broader than anticipated.