Elsevier

Neuroscience

Volume 277, 26 September 2014, Pages 435-445
Neuroscience

Motion perception correlates with volitional but not reflexive eye movements

https://doi.org/10.1016/j.neuroscience.2014.07.028Get rights and content

Highlights

  • Examined inter-individual variability in eye movements and direction perception.

  • Precision of ocular following and smooth pursuit was correlated across observers.

  • Across observers, perceptual precision correlated with smooth pursuit precision.

  • Perceptual precision was uncorrelated with ocular following precision.

Abstract

Visually-driven actions and perception are traditionally ascribed to the dorsal and ventral visual streams of the cortical processing hierarchy. However, motion perception and the control of tracking eye movements both depend on sensory motion analysis by neurons in the dorsal stream, suggesting that the same sensory circuits may underlie both action and perception. Previous studies have suggested that multiple sensory modules may be responsible for the perception of low- and high-level motion, or the detection versus identification of motion direction. However, it remains unclear whether the sensory processing systems that contribute to direction perception and the control of eye movements have the same neuronal constraints. To address this, we examined inter-individual variability across 36 observers, using two tasks that simultaneously assessed the precision of eye movements and direction perception: in the smooth pursuit task, observers volitionally tracked a small moving target and reported its direction; in the ocular following task, observers reflexively tracked a large moving stimulus and reported its direction. We determined perceptual–oculomotor correlations across observers, defined as the correlation between each observer’s mean perceptual precision and mean oculomotor precision. Across observers, we found that: (i) mean perceptual precision was correlated between the two tasks; (ii) mean oculomotor precision was correlated between the tasks, and (iii) oculomotor and perceptual precision were correlated for volitional smooth pursuit, but not reflexive ocular following. Collectively, these results demonstrate that sensory circuits with common neuronal constraints subserve motion perception and volitional, but not reflexive eye movements.

Introduction

Visual processing in the brain subserves two related purposes: guiding actions and informing perception. In the visual cortical hierarchy, these roles are often separately ascribed to the dorsal and ventral streams, respectively (Ungerleider and Mishkin, 1982, Goodale and Milner, 1992). Motion processing provides an excellent system for examining links between action and perception within a single stream, as it is traditionally associated with sensory processing by dorsal-stream neurons in the middle temporal area (MT) and medial superior temporal area (MST) (Born and Bradley, 2005). It is well established that MT/MST neurons drive volitional smooth pursuit (SP) eye movements (Komatsu and Wurtz, 1989), reflexive ocular following (OF) eye movements (Kawano et al., 1994, Ibbotson et al., 2007), and motion perception (Newsome and Pare, 1988, Britten et al., 1996). However, it remains unclear whether motion perception and the control of eye movements have overlapping computational constraints, and whether overlapping circuits control volitional and reflexive movements.

If motion perception and eye movements depend on shared sensory processing, errors in an observer’s perceptual and oculomotor performance might be correlated across trials. Such correlations have been reported between SP and direction perception (Krauzlis and Adler, 2001, Stone and Krauzlis, 2003), but not for tasks requiring speed judgments during pursuit (Gegenfurtner et al., 2003, Tavassoli and Ringach, 2010), or during OF (Bostrom and Warzecha, 2010, Spering et al., 2011, Blum and Price, 2014, Glasser and Tadin, 2014). The presence of correlations in only some studies is attributable to a range of causes, including: (1) noise downstream from the region of common processing overwhelming any measurable correlation; (2) perceptual task differences (e.g. direction versus speed judgments); (3) oculomotor task differences (e.g. reflexive versus volitional movements); (4) efference copy modifying sensory processing; and (5) eye movements impairing perception (Schutz et al., 2011, Spering and Montagnini, 2011). Any of these conditions would make it more difficult to observe correlated variability between two tasks, even when those tasks depend on common sensory neurons.

One way to overcome these limitations is to compare variability across observers, rather than across trials performed by a single observer. Individual differences studies have demonstrated that an observer’s performance on one perceptual task can predict their performance “within-domains” on other perceptual tasks, and “between-domains” on motor tasks (Wilmer and Nakayama, 2007, Wilmer, 2008). These results are interpreted as evidence that the same neural circuit, or neural systems with common processing constraints, are involved in each task (Halpern et al., 1999, Kosslyn et al., 2002, Wilmer, 2008).

We compared the precision of motor responses (SP and OF) and direction perception. We primarily assessed perceptual–oculomotor correlations, defined as the across-observers correlation between each observer’s mean perceptual precision and mean oculomotor precision. We show that performance on perceptual and volitional behavioral tasks is correlated, whereas performance on perceptual and reflexive behavioral tasks is not correlated. While different requirements for the spatial integration of motion may account for the differences between OF and pursuit, our results suggest that sensory circuits with common neural constraints perform the motion analysis for action and perception.

Section snippets

Participants

Thirty-nine volunteers (21 females, 18 males; ages 18–65) with normal or corrected to normal vision participated in the experiment. All had no, or limited, prior psychophysical experience. Fifteen observers participated as part of an undergraduate project and the remainder were compensated for their time. Before data collection commenced all observers completed ∼20 trials of each task to familiarize themselves with the stimulus and methods. Data from three participants were excluded due to the

Results

We compared the oculomotor and perceptual precision of 36 participants in SP and OF tracking tasks. In the SP task, participants volitionally tracked a small target and subsequently reported its motion direction (Fig. 1A). In the OF task, participants reflexively tracked a large field of moving dots and subsequently reported the motion direction (Fig. 1B). In both tasks, the direction of motion was randomly selected on each trial.

Discussion

The hierarchy of cortical visual areas is typically divided into parallel dorsal and ventral streams, which have been associated with performing the sensory analysis underlying vision for action and perception, respectively (Ungerleider and Mishkin, 1982, Goodale and Milner, 1992). Many studies have examined both the interdependence and separability of processing in the two streams; however, this dichotomy is not strictly relevant to the control of smooth eye movements and motion perception, as

Conclusion

Previous electrophysiological and behavioral work has established that perception, SP and OF all depend on motion analysis performed by MT/MST neurons. Here, we assess whether the neural circuits that mediate action and perception are subject to the same neural constraints. We argue that different modules within MT/MST are responsible for perception and action; these comprise overlapping sets of sensory neurons with distinct read-out circuitry. This is consistent with previous work showing that

Acknowledgments

This work was supported by NHMRC Project grant APP1008287, an HFSP Career Development Award and a Ramaciotti Equipment Grant. We thank Adam Morris and Liz Zavitz for comments on the manuscript. The authors declare no competing financial interests.

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