Single-neuron activity in the dorsomedial frontal cortex during smooth-pursuit eye movements to predictable target motion

Heinen, Stephen; Liu, M.

doi:10.1017/s0952523800011597

Cited by 104 publications

(95 citation statements)

References 44 publications

(66 reference statements)

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“…We have found activation in this area previously for both types of eye movement when making predictive eye movements to a single target (Burke & Barnes, 2008). Other studies have found this area has been mainly associated with very short-term memory acquisition for single target locations (Heinen & Liu, 1997), and one previous study with prediction (Schmid et al, 2001). Our MVPA results demonstrate that this area is important in both saccades and pursuit during early motor learning for a series of movements.…”

Section: Multivariate Analysissupporting

confidence: 74%

The involvement of the fronto-parietal brain network in oculomotor sequence learning using fMRI

2016

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The basis of motor learning involves decomposing complete actions into a series of predictive individual components that form the whole. The present fMRI study investigated the areas of the human brain important for oculomotor short-term learning, by using a novel sequence learning paradigm that is equivalent in visual and temporal properties for both saccades and pursuit, enabling more direct comparisons between the oculomotor subsystems. In contrast with previous studies that have implemented a series of discrete ramps to observe predictive behaviour as evidence for learning, we presented a continuous sequence of interlinked components that better represents sequences of actions. We implemented both a classic univariate fMRI analysis, followed by a further multivariate pattern analysis (MVPA) within a priori regions of interest, to investigate oculomotor sequence learning in the brain and to determine whether these mechanisms overlap in pursuit and saccades as part of a higher order learning network. This study has uniquely identified an equivalent frontal-parietal network (dorsolateral prefrontal cortex, frontal eye fields and posterior parietal cortex) in both saccades and pursuit sequence learning. In addition, this is the first study to investigate oculomotor sequence learning during fMRI brain imaging, and makes significant contributions to understanding the role of the dorsal networks in motor learning.

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Section: Multivariate Analysissupporting

confidence: 74%

The involvement of the fronto-parietal brain network in oculomotor sequence learning using fMRI

2016

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“…Pursuit-related neurons are found in the cerebral cortex including the medial superior temporal visual area, frontal and supplementary eye fields, and ventral intra-parietal area (Sakata et al 1983;MacAvoy et al 1991;Colby et al 1993;Heinen and Liu 1997;Bremmer et al 2002;. Although upward and downward optic flows may be different in the natural environment, preferred directions for individual pursuit neurons in these cortical areas are distributed virtually evenly for all directions, making it difficult to explain the directional asymmetry observed in our study solely on the basis of cortical smooth-pursuit mechanisms .…”

Section: Possible Neural Correlates For the Directional Asymmetry In mentioning

confidence: 68%

“…Our laboratory has reported that chemical inactivation of the supplementary eye fields (SEF) in adult monkeys reproduced the directional asymmetry that had been compensated developmentally, suggesting that the SEF may be involved in the compensation . Although the exact neural mechanisms for the compensation and reappearance of the directional asymmetry induced by SEF inactivation are still unknown, preferred directions for individual SEF pursuit neurons are distributed virtually evenly for all directions (Heinen and Liu 1997;Fukushima et al 2004). Therefore, it is difficult to explain the reproduced directional asymmetry solely by loss of SEF output signals.…”

Section: For Dorsal Vermis Purkinje Cells) the Floccular Region Consmentioning

confidence: 99%

Further evidence for selective difficulty of upward eye pursuit in juvenile monkeys: effects of optokinetic stimulation, static roll tilt, and active head movements

et al. 2005

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The smooth-pursuit system moves the eyes in space accurately to track slowly moving objects of interest despite visual inputs from the moving background and/or vestibular inputs during head movements. Recently, our laboratory has shown that young primates exhibit asymmetric eye movements during vertical pursuit across a textured background; upward eye velocity gain is reduced. To further understand the nature of this asymmetry, we performed three series of experiments in young monkeys. In Experiment 1, we examined whether this asymmetry was due to an un-compensated downward optokinetic reflex induced by the textured background as it moves across the retina in the opposite direction of the pursuit eye movements. For this, we examined the monkeys’ ability to fixate a stationary spot in space during movement of the textured background and compared it with vertical pursuit across the stationary textured background. We also examined gains of optokinetic eye movements induced by downward motion of the textured background during upward pursuit. In both task conditions, gains of downward eye velocity induced by the textured background were too small to explain reduced upward eye velocity gains. In Experiment 2, we examined whether the frame of reference for low-velocity, upward pursuit was orbital or earth vertical. To test this, we first applied static tilt in the roll plane until the animals were nearly positioned on their side in order to dissociate vertical or horizontal eye movements in the orbit from those in space. Deficits were observed for upward pursuit in the orbit but not in space. In Experiment 3, we tested whether asymmetry was observed during head-free pursuit that requires coordination between eye and head movements. Asymmetry in vertical eye velocity gains was still observed during head-free pursuit although it was not observed in vertical head velocity. These results, taken together, suggest that the asymmetric eye movements during vertical pursuit are specific for upward, primarily eye pursuit in the orbit

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“…It acts as a timer, with activity that rises during the course of a trial. This process is based on activity recorded in SEF from preparatory or anticipation cells (Heinen and Liu, 1997). The fixation and anticipation components in the model interact in a mutually inhibitory manner.…”

Section: Discussionmentioning

confidence: 99%

Anticipatory Movement Timing Using Prediction and External Cues

Badler¹,

Heinen²

2006

J. Neurosci.

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Animals often make anticipatory movements to compensate for slow reaction times. Anticipatory movements can be timed using external, sensory cues, or by an internal prediction of when an event will occur. However, it is unknown whether external or internal cues dominate the anticipatory response when both are present. Smooth pursuit eye movements are generated by a motor system heavily influenced by anticipation. We measured pursuit to determine how its timing was influenced when both a predictable event and a visual cue were present. Monkeys tracked a moving target that appeared at a constant time relative to the onset of a fixation point. At a randomized time before target onset, the fixation point disappeared, creating a temporal "gap" that cued impending target motion. We found that the gap onset cue and prediction of target onset together determined pursuit initiation time. We also investigated whether prediction could override the gap onset cue or vice versa by manipulating target onset and, hence, the duration of time that the animal had to estimate to predict it. When target motion began earlier, the pursuit system relied more on prediction to trigger a movement, whereas the cue was more often used when the target moved later. Pursuit latency in previous trials partially accounted for this behavior. The results suggest that neither internal nor external factors dominate to control the anticipatory response and that the relative contributions vary with stimulus conditions. A model in which neuronal anticipation and fixation signals interact can explain the results.

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Single-neuron activity in the dorsomedial frontal cortex during smooth-pursuit eye movements to predictable target motion

Cited by 104 publications

References 44 publications

The involvement of the fronto-parietal brain network in oculomotor sequence learning using fMRI

The involvement of the fronto-parietal brain network in oculomotor sequence learning using fMRI

Further evidence for selective difficulty of upward eye pursuit in juvenile monkeys: effects of optokinetic stimulation, static roll tilt, and active head movements

Anticipatory Movement Timing Using Prediction and External Cues

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