Adaptation accentuates responses of fly motion-sensitive visual neurons to sudden stimulus changes

Abstract

Adaptation in sensory and neuronal systems usually leads to reduced responses to persistent or frequently presented stimuli. In contrast to simple fatigue, adapted neurons often retain their ability to encode changes in stimulus intensity and to respond when novel stimuli appear. We investigated how the level of adaptation of a fly visual motion-sensitive neuron affects its responses to discontinuities in the stimulus, i.e. sudden brief changes in one of the stimulus parameters (velocity, contrast, grating orientation and spatial frequency). Although the neuron's overall response decreased gradually during ongoing motion stimulation, the response transients elicited by stimulus discontinuities were preserved or even enhanced with adaptation. Moreover, the enhanced sensitivity to velocity changes by adaptation was not restricted to a certain velocity range, but was present regardless of whether the neuron was adapted to a baseline velocity below or above its steady-state velocity optimum. Our results suggest that motion adaptation helps motion-sensitive neurons to preserve their sensitivity to novel stimuli even in the presence of strong tonic stimulation, for example during self-motion.

Octopaminergic modulation of a fly visual motion-sensitive neuron during stimulation with naturalistic optic flow

“…Stimulus-specific differences in the strength of adaptation, which may be relevant in the context of octopaminergic modulation, were also demonstrated in a previous study (Kurtz et al, 2009). In this study, the H1 neuron was driven into a strongly adapted state by sustained grating motion with constant properties and then challenged by sudden changes in one of the stimulus properties (velocity, direction, luminance contrast, or pattern wavelength).…”

Spatial vision in insects is facilitated by shaping the dynamics of visual input through behavioral action

“…All these processes are usually regarded as adaptive, although their functional significance is still not entirely clear. Several non-exclusive possibilities have been proposed, such as adjusting the dynamic range of motion sensitivity to the prevailing stimulus dynamics (Brenner et al, 2000a; Fairhall et al, 2001), saving energy by adjusting the neural response amplitudes without affecting the overall information that is conveyed (Heitwerth et al, 2005), and increasing the sensitivity to changes in stimulus parameters resulting from environmental discontinuities (Maddess and Laughlin, 1985; Liang et al, 2008, 2011; Kurtz et al, 2009). …”

A simple canonical circuitry for non-stationary normalization by inhibition to explain and predict change detection in monkey area MT

“…Neuronal responses to fast stimulus transitions usually come as brief episodes of increased or decreased neuronal activity, followed by a steady-state level of lower absolute amplitude. Pronounced transient changes in neuronal activation were observed in the brain of many different species, spanning the range from invertebrates to primates [23][24][25] , suggesting that they represent a basic principle in neuronal network dynamics. We here show that such a canonical computation can be realized by a very simple circuitry, essentially built of only one excitatory and one inhibitory unit, in which the excitatory unit's output time course is normalized through divisive inhibition.…”