Motion adaptation reveals that the motion vector is represented in multiple coordinate frames

Abstract

Accurately perceiving the velocity of an object during smooth pursuit is a complex challenge: although the object is moving in the world, it is almost still on the retina. Yet we can perceive the veridical motion of a visual stimulus in such conditions, suggesting a nonretinal representation of the motion vector. To explore this issue, we studied the frames of representation of the motion vector by evoking the well known motion aftereffect during smooth-pursuit eye movements (SPEM). In the retinotopic configuration, due to an accompanying smooth pursuit, a stationary adapting random-dot stimulus was actually moving on the retina. Motion adaptation could therefore only result from motion in retinal coordinates. In contrast, in the spatiotopic configuration, the adapting stimulus moved on the screen but was practically stationary on the retina due to a matched SPEM. Hence, adaptation here would suggest a representation of the motion vector in spatiotopic coordinates. We found that exposure to spatiotopic motion led to significant adaptation. Moreover, the degree of adaptation in that condition was greater than the adaptation induced by viewing a random-dot stimulus that moved only on the retina. Finally, pursuit of the same target, without a random-dot array background, yielded no adaptation. Thus, in our experimental conditions, adaptation is not induced by the SPEM per se. Our results suggest that motion computation is likely to occur in parallel in two distinct representations: a low-level, retinal-motion dependent mechanism and a high-level representation, in which the veridical motion is computed through integration of information from other sources.

Spatiotopic updating across saccades revealed by spatially-specific fMRI adaptation

“…While both theories would predict effects in frontal-parietal saliency maps (although attentional pointers should result in enhanced rather, than suppressed, activity), only the object pointer theory (Melcher & Colby, 2008) would predict spatial updating in visual areas. Indeed, spatial updating in visual areas would seem to be important to explain spatiotopic visual effects, such as feature integration ((Hayhoe et al, 1991;Melcher & Morrone, 2003;Prime et al, 2006;Gordon et al, 2008;Van Eccelpoel et al, 2008;Wittenberg et al, 2008;Demeyer et al, 2009;Fracasso et al, 2010;Demeyer et al, 2011;Melcher & Fracasso, 2012;Fabius et al, 2016) or feature adaptation (Melcher, 2005;Ong et al, 2009;Biber & Ilg, 2011;Seidel Malkinson et al, 2012;Zimmermann et al, 2013;Cha & Chong, 2014;Wolfe & Whitney, 2015). One of the criticisms of previous behavioral studies showing spatiotopic effects is that visual areas are obviously retinotopic, calling into question whether these effects are neurally plausible.…”

Nonretinotopic visual processing in the brain

“…Another of the main findings in these behavioral studies is that perceptual reports are consistent with the transfer/integration of feature information across saccades. Examples include the perception of shape/orientation/form (Hayhoe et al, 1991; Melcher, 2005; Prime et al, 2006, 2011; Melcher, 2007; Gordon et al, 2008; Van Eccelpoel et al, 2008; Demeyer et al, 2009, 2010, 2011; Fracasso et al, 2010; Zirnsak et al, 2011; Zimmermann et al, 2013 a , b ; Cha & Chong, 2014), color (Wittenberg, Bremmer & Wachtler, 2008), motion (Melcher & Morrone, 2003; Ong et al, 2009; Fracasso et al, 2010; Biber & Ilg, 2011; Melcher & Fracasso, 2012; Seidel Malkinson et al, 2012; Turi & Burr, 2012) and perceived time duration (Burr et al, 2007). A key similarity of these different studies is that perceptual responses are based on combining information from different retinal locations, and this requires the alignment of the visual information in external (spatiotopic) coordinates or the alignment of the presaccadic and postsaccadic locations of an object.…”

“…Given that these two stimuli can interact perceptually in various ways, such as priming, integration, adaptation, and so on, the presence of such interactions can be used as evidence for nonretinotopic processing and in particular for spatiotopic effects. A large number of studies have reported spatiotopic effects (Hayhoe et al, 1991; Melcher & Morrone, 2003; Melcher, 2005, 2007, 2009; Prime et al, 2006, 2011; Burr et al, 2007; Ezzati et al, 2008; Gordon et al, 2008; Van Eccelpoel et al, 2008; Wittenberg et al, 2008; Demeyer et al, 2009, 2010, 2011; Ong et al, 2009; Fracasso et al, 2010; Fracasso et al, 2010; Biber & Ilg, 2011; Burr et al, 2011; Au et al, 2012; Melcher & Fracasso, 2012; Seidel Malkinson et al, 2012; Turi & Burr, 2012; Zimmermann et al, 2013 a , b ; Cha & Chong, 2014; Corbett & Melcher, 2014; Jonikaitis & Belopolsky, 2014; Nakashima & Sugita, 2014), while other studies have found only retinotopic effects (Wenderoth & Wiese, 2008; Afraz & Cavanagh, 2009; Knapen et al, 2009). As will be described below, this difference might result from various causes, including: the level of the cortical processing involved, the dynamics of the presentation of the stimuli, the attentional state of the subject, the memory load and the predictions and expectations of the subject.…”

“…Given that these two stimuli can interact perceptually in various ways, such as priming, integration, adaptation, and so on, the presence of such interactions can be used as evidence for nonretinotopic processing and in particular for spatiotopic effects. A large number of studies have reported spatiotopic effects (Hayhoe et al, 1991 ;Melcher & Morrone, 2003 ;Melcher, 2005Melcher, , 2007Melcher, , 2009Prime et al, 2006Prime et al, , 2011Burr et al, 2007 ;Ezzati et al, 2008 ;Gordon et al, 2008 ;Van Eccelpoel et al, 2008 ;Wittenberg et al, 2008 ;Demeyer et al, 2009Demeyer et al, , 2010Demeyer et al, , 2011Ong et al, 2009 ;Fracasso et al, 2010 ;Fracasso et al, 2010 ;Biber & Ilg, 2011 ;Au et al, 2012 ;Melcher & Fracasso, 2012 ;Seidel Malkinson et al, 2012 ;Turi & Burr, 2012 ;Zimmermann et al, 2013 a , b ;Cha & Chong, 2014 ;Corbett & Melcher, 2014 ;Jonikaitis & Belopolsky, 2014 ;Nakashima & Sugita, 2014 ), while other studies have A change in gaze position from the right side of an object to the left side of an object, via a horizontal saccade, would create a situation in which the neural processing of that object in visual areas would switch hemispheres, involving a completely new set of neurons. Nonetheless, our subjective perception of the object is that it remains stable in external space and identity across the gaze shift.…”

Effect of spatial attention on spatiotopic visual motion perception

“…A standard way of examining the spatiotopic effect is to present an observer with two stimuli over time in the same spatial (screen-based) position, separated by a saccade that causes the two stimuli to fall in different retinal locations (Melcher, 2005;Melcher & Colby, 2008;Melcher & Morrone, 2015). Preparing two moving stimuli and examining whether these moving stimuli interact through adaptation or priming would help us to understand the characteristics of spatiotopic effects on visual motion perception (Biber & Ilg, 2011;Burr, Cicchini, Arrighi, & Morrone, 2011;Burr, Tozzi, & Morrone, 2007;Ezzati, Golzar, & Afraz, 2008;Fracasso, Caramazza, & Melcher, 2010;Knapen et al, 2009;Melcher & Fracasso, 2012;Melcher & Morrone, 2003;Ong, Hooshvar, Zhang, & Bisley, 2009;Seidel Malkinson, Mckyton, & Zohary, 2012;Turi & Burr, 2012;Wenderoth & Wiese, 2008;Yoshimoto, Uchida-Ota, & Takeuchi, 2014a;Yoshimoto, Uchida-Ota, & Takeuchi, 2014b; see summary by Marino & Mazer, 2016, table 3). In this study, consequently, we used the visual motion priming paradigm (Ong et al, 2009;Yoshimoto et al, 2014a;Yoshimoto et al, 2014b) in addition to concurrently conducting a dot contrast-change detection task (Crespi et al, 2011) to control the spatial attention of spatiotopic motion perception.…”