Elsevier

Cortex

Volume 98, January 2018, Pages 228-248
Cortex

Special issue: Review
Do we have distinct systems for immediate and delayed actions? A selective review on the role of visual memory in action

https://doi.org/10.1016/j.cortex.2017.05.014Get rights and content

Abstract

The perception-action model with its assumptions of distinct visual pathways for perception and visuomotor control has been highly influential but also contentious. The controversy largely focused on the evidence from studies on perceptual illusions and this scientific field has been reviewed quite a few times in recent years. In contrast another aspect of the model, namely the role of visual memory in action control, received comparatively little attention. With respect to visual memory the perception-action model proposes that only the perceptual or ventral stream can maintain a sustained representation of the visual world while the visuomotor system or dorsal stream has to rely on currently available visual information. Consequently, visual information from the dorsal system cannot guide actions that are based on memorized visual information. We call this feature of the perception-action model: the dorsal amnesia hypothesis. There are at least two reasons for why this hypothesis is of special relevance. Firstly, it provides a particularly clear criterion to distinguish between functions of the ventral and dorsal stream. Secondly, this hypothesis led to some unexpected discoveries which provided particularly compelling evidence in favour of the model. In this review, we will revisit all relevant empirical areas, ranging from physiological examinations and neuropsychological studies to behavioural experiments in neurologically intact participants. Based on this review, we conclude that the dorsal amnesia hypothesis is in our view no longer tenable.

Section snippets

A visual path with no memory? Evidence from neurophysiology, fMRI and TMS

The dorsal amnesia hypothesis assumes that visual representations in the dorsal stream are too transient to support memory-based actions. Both electrophysiological recordings from dorsal-stream neurons in non-human primates and fMRI studies on cortical areas situated in the dorsal stream can be consulted to address this question. The few non-human primate studies that have looked directly at the time-course of spiking activity in parietal regions associated with visually guided hand movements

Trapped in the present. How ventral-stream damage affects memory-based action

The conclusion that ventral stream damage impairs the ability to perform memory-based visuomotor acts received initial support from a classic study conducted by Goodale, Jakobson, et al. (1994a). In this study, DF was first asked to grasp target objects placed in front of her. Her ability to adjust her hand-opening to the objects' size seemed normal. Next, she was again asked to grasp objects but this time vision of the target object was removed as well as the object itself. After a delay of

Stuck in the past: how dorsal-stream damage affects memory-based action

Optic ataxia is a comparatively rare but very interesting and to some extent puzzling disorder. First described by Bálint (1909) it forms part of the so-called Balint-Holmes syndrome which is sometimes observed in the context of neuronal damage to posterior portions of the parietal cortex (Goethals & Santens, 2001). This type of neuronal damage can occur as a result of stroke but also in the course of neurodegenerative disorders such as posterior cortical atrophy, a form of dementia. Patients

Dorsal amnesia: how reliance on memory impairs actions in neurologically intact humans

An interesting consequence of the formulation of the perception-action model (Goodale and Milner, 1992, Milner and Goodale, 1995, Milner and Goodale, 2006) was an increased arousal of interest in the investigation of the relationship between visual factors and manual control, a topic that had been until then largely neglected by psychologists (see, Rosenbaum, 2005). Interestingly, however, it is often ignored that the question of how humans use visual information to control voluntary movements

Visual illusions, actions and delays

Evidence for the suggestion that the altered movement kinematics after delay are indeed a result of degraded visual information comes from studies investigating the effect of visual illusion on reaching and grasping kinematics in different vision conditions (e.g., Gentilucci et al., 1996, Hu and Goodale, 2000, Westwood and Goodale, 2003, Westwood et al., 2000, Westwood et al., 2001b). In short, the rationale of these studies is that when vision is available during the movement (or at least

The role of allocentric and egocentric cues for the visual guidance of actions

The underlying assumption of why visual illusions affect movements performed after delay but not in real time is that, according to the perception-action model, the long-lasting information represented within the ventral stream maintains information in an allocentric frame of reference (taking the environmental context into account). In contrast, the real-time information maintained in the dorsal stream is supposed to be represented in an egocentric frame of reference (relative to the

Summary and conclusions

In this article we focused on one specific aspect of the perception-action model, its claim of the transient nature of the visual information processed in the dorsal stream. This claim, which we called the dorsal amnesia hypothesis, led to some interesting predictions and findings and received support from a wide range of different scientific domains. In this review, we critically re-examined the evidence from those different domains. We come to the conclusion that neither the findings from

Acknowledgements

Thomas Schenk was supported by grants from the German Research Foundation (Deutsche Forschungsgemeinschaft, DFG, grant no's: DFG-SCHE 735/2-1 and DFG-SCHE 735/3-1).

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