Perceptual and neural consequences of rapid motion adaptation

Abstract

Nervous systems adapt to the prevailing sensory environment, and the consequences of this adaptation can be observed in the responses of single neurons and in perception. Given the variety of timescales underlying events in the natural world, determining the temporal characteristics of adaptation is important to understanding how perception adjusts to its sensory environment. Previous work has shown that neural adaptation can occur on a timescale of milliseconds, but perceptual adaptation has generally been studied over relatively long timescales, typically on the order of seconds. This disparity raises important questions. Can perceptual adaptation be observed at brief, functionally relevant timescales? And if so, how do its properties relate to the rapid adaptation seen in cortical neurons? We address these questions in the context of visual motion processing, a perceptual modality characterized by rapid temporal dynamics. We demonstrate objectively that 25 ms of motion adaptation is sufficient to generate a motion aftereffect, an illusory sensation of movement experienced when a moving stimulus is replaced by a stationary pattern. This rapid adaptation occurs regardless of whether the adapting motion is perceived. In neurophysiological recordings from the middle temporal area of primate visual cortex, we find that brief motion adaptation evokes directionselective responses to subsequently presented stationary stimuli. A simple model shows that these neural responses can explain the consequences of rapid perceptual adaptation. Overall, we show that the motion aftereffect is not merely an intriguing perceptual illusion, but rather a reflection of rapid neural and perceptual processes that can occur essentially every time we experience motion.T he nervous system constantly adapts to the statistics of its sensory inputs, and such adaptation has important perceptual consequences (1, 2). Examples include the desensitization of the somatosensory system to constant stimuli (e.g., clothing) and the visual system's adjustments to prevailing light levels. Adaptation affects both neural activity during constant stimulation and neural responses to subsequent stimuli (1). Given the variety of timescales underlying events in the natural world, determining the temporal characteristics of adaptation is a key step in understanding sensory perception. Traditionally, perceptual adaptation is thought to occur over long time periods, with the adapting stimuli being presented for seconds or longer. Neurophysiological work, however, has shown that adaptation occurs at a variety of timescales and can be observed following stimulus exposures as brief as tens of milliseconds (1, 3-7). This rapid adaptation has strong implications for neural coding of sensory stimuli (5,6,8), which renders the relative lack of evidence about brief perceptual adaptation puzzling. Here we consider this question in the context of visual motion processing. Because of the highly dynamic nature of moving stimuli, rapid adaptation is potentially of great relev...

Modelling fast forms of visual neural plasticity using a modified second-order motion energy model

“…On the other hand, following longer exposure to directional motion the sensor signals a direction opposite to the adapting pattern (i.e., rMAE). Thus, the final output of the second-order model shows effects which mirror those reported by previous psychophysical studies on fast forms of motion adaptation (Kanai and Verstraten 2005;Pavan et al 2009Pavan et al , 2010Glasser et al 2011;Pavan and Skujevskis 2013). The extended Motion Energy Model does not account for another effect previously reported by Kanai and Verstraten (2005) and Pavan et al (2009Pavan et al ( , 2010, called "Perceptual Sensitization" (PS).…”

“…When two stimuli are presented in rapid succession, the neural response to the latter stimulus is considerably reduced, a phenomenon well known as short-term synaptic depression (Nelson 1991;Finlayson and Cynader 1995;Varela et al 1997Varela et al , 1999Chance et al 1998;Lisberger and Movshon 1999;Boudreau and Ferster 2005). Short-term synaptic depression has been reported within the striate cortex of cats (Boudreau and Ferster 2005) and also in area MT of monkeys (Lisberger and Movshon 1999;Glasser et al 2011). , for example, found that monkey MT neurons respond to a motion step with a transient-sustained firing rate.…”

“…Very brief exposure to directional stimuli can bias the perceived motion direction of a subsequently presented ambiguous test pattern (Kanai and Verstraten 2005;Pavan et al 2009;Glasser et al 2011;Pavan and Skujevskis 2013). In particular, depending on both the duration of the adaptation pattern and the duration of the blank inter-stimulus interval (ISI) between adaptation and testing, the perceived direction of an ambiguous test pattern can be biased towards the opposite direction (after-effect), or towards the same direction (priming) of the adaptation pattern (Pinkus and Pantle 1997).…”

“…The transition from an initial high firing rate to a lower sustained rate occurs over a temporal window of 20-80 ms and can be considered as a form of shortterm adaptation. Accordingly, Glasser et al (2011) found that in monkey MT a very brief exposure to directional motion (67 ms) produced direction-selective responses to subsequently presented stationary test stimuli. This is also compatible with a short-term form of motion adaptation.…”

Individual differences in visual motion perception and neurotransmitter concentrations in the human brain

“…Neurophysiological studies have shown that a moving stimulus with a very short duration, such as several hundred milliseconds, is sufficient to change the adaptation status of directionally selective neurons located at V1 [46]. This type of rapid adaptation of directionally selective neurons is assumed to be an underlying mechanism of motion contrast (or rMAE) [47]. In contrast with our study, van Loon et al [3] found that the GABA concentration in the V1, but not the Glx concentration in the PFC, is correlated with the dynamics of visual bistable perception.…”