Kevin A. Briand

Control of voluntary and reflexive saccades in Parkinson’s disease

Abstract Eight patients with idiopathic Parkinson’s disease (PD) were compared with a group of age-matched controls on both reflexive saccade and antisaccade tasks. While reflexive, visually guided saccades led to equivalent performance in both groups, PD patients were slower, made more errors, and showed reduced gain on antisaccades (AS). This is consistent with previous results showing that PD patients have no difficulty with reflexive saccades but show deficiencies in a number of voluntary saccade paradigms. Moreover, visual information in the form of landmarks improves AS performance more for PD patients than controls, a finding analogous to results seen with other motor acts such as target-directed pointing. Results are discussed in terms of a two-process model of attention and eye movements.

Inhibition of return in manual and saccadic response systems

When nonpredictive exogenous visual cues are used to reflexively orient covert visual spatial attention, the initial early facilitation for detecting stimuli at cued versus uncued spatial locations develops into inhibition by 300 msec following the cue, a pattern referred to asinhibition of return (IOR). Experiments were carried out comparing the magnitude and time course for development of IOR effects when manual versus saccadic responses were required. The results showed that both manual and saccadic responses result in equivalent amounts of facilitation following initial exposure to a spatial cue. However, IOR developed more quickly for saccadic responses, such that, at certain cue-target SO As, saccadic responses to targets were inhibited, whereas manual responses were still facilitated. The findings are interpreted in terms of a premotor theory of visual attention.

Levodopa slows prosaccades and improves antisaccades: an eye movement study in Parkinson’s disease

Background: The integrity of frontal systems responsible for voluntary control and their interaction with subcortical regions involved in reflexive responses were studied in patients with Parkinson’s disease (PD). Previous studies have shown that patients with PD have impaired executive function, including deficits in attention, motor planning and decision making. Methods: Executive function was measured through eye movements: reflexive (stimulus driven) prosaccades and voluntary (internally guided) antisaccades. Patients with advanced idiopathic PD, off and on their optimal levodopa therapy, were tested on a prosaccade and an antisaccade task and compared with matched controls. Results: Levodopa significantly increased response time for reflexive prosaccades and reduced error rate for voluntary antisaccades. Conclusions: Consistent with our proposed model, patients with PD in the medicated state are better able to plan and execute voluntary eye movements. These findings suggest levodopa improves function of the voluntary frontostriatal system, which is deficient in PD.

Schizotypal traits, attention and eye movements

1. Subjects demonstrating high, average, or low schizotypal traits participated in saccade tasks of eye movements and attention including: a simple saccade task, an antisaccade task, and/or a cued saccade task measuring both facilitatory effects of cuing and inhibition of return (IOR). 2. Subjects were recruited based on their scores on the Rust Inventory of Schizotypal Cognitions (RISC) and then were given Raines Schizotypal Personality Questionnaire (SPQ) (1991). 3. Subjects scoring high in schizotypy demonstrated increased errors on the voluntary eye movement task (antisaccade task) (p<0.05). Performance on the reflexive saccade task was not impaired in high compared to low schizotypals, but may have been enhanced as demonstrated by a negative correlation between scores on the SPQ and performance on this task. For the cued saccade task, there were no overall differences in cueing effects between schizotypal groups, however there was a laterality difference between low versus high scoring schizotypal subjects. 4. These results indicate distinct differences in tasks of overt orienting (saccade and antisaccade tasks) and covert orienting tasks (cued saccade task). The patterns of performance by our schizotypy subjects, including impaired voluntary saccade, enhanced reflexive saccade, and lateralized performance on the cued saccade task, are consistent with the performance of schizophrenic patient populations. Thus, our study supports the previous findings of a physiological relationship between schizotypal personality and schizophrenia.

The role of response in spatial attention: direct versus indirect stimulus-response mappings

Recent research has suggested that inhibition of return (IOR) develops more quickly when subjects must respond with an eye movement than when they make a manual response to the target (Perception and Psychophysics 62 (2000) 1512-1524). Four spatial cueing experiments were conducted where subjects had to indicate the location of visual targets. Within each of the oculomotor and manual modalities, responses could be either directed towards the target (saccade or pointing) or had a more complex stimulus-response (S-R) mapping. For both saccadic and manual responses, IOR onset was delayed as the required S-R mapping became more indirect. This finding further emphasizes the role of response-related processes in spatial attention. Possible explanations for this pattern of results are considered, including the notion that activity in prefrontal cortex, needed for execution of such abstract S-R mappings, may influence the time course of reflexive spatial cueing effects.

Disruption of Reflexive Attention and Eye Movements in an Individual with a Collicular Lesion

The superior colliculus (SC) plays a central role in the control of saccadic eye movements and has also been implicated in control of covert spatial attention. While there is a growing body of evidence from studies of awake behaving primates that supports these proposals, direct evidence from humans has been sparse. In the present study we tested a patient with thiamine deficiency and a lesion of the SC, who performed both eye movement tasks (prosaccades and antisaccades, with or without a gap) and a covert spatial attention task assessing inhibition of return (IOR). For eye movements, the gap effect was disrupted, and abnormal saccade metrics occurred, with reflexive eye movements being disrupted moreso than voluntary eye movements. Each of these effects resolved coincident with thiamine treatment. The covert attention task revealed a complete absence of IOR. The unequal disruption of voluntary and reflexive eye movements supports the idea that oculomotor responses can be generated in an independent fashion by frontal cortical and lower level neural systems. The role of the SC and other structures in these orienting processes is discussed.

Delayed onset of inhibition of return in schizophrenia

Peripheral visual cues occuring before a subsequent target result in an almost immediate facilitatory and then a later inhibitory effect on target detection. In a detailed parametric investigation, the authors compared schizophrenic subjects (SCZ) and control subjects (CONT) to examine whether they showed any differences in the time course of these nonpredictive peripheral cuing effects. Subjects fixated a central position and made saccadic responses to visual targets. Targets were presented 10 degrees to the left or right of fixation and were preceded at various time intervals by visual cues. Targets occurred with equal probability in either the same position as the cue or in the opposite, uncued location, and 10 delay periods were used corresponding to stimulus onset asynchronies (SOAs) of 66, 79, 106, 133, 159, 226, 305, 505, 705, and 1000 ms. All subjects showed facilitation for short cue-target delays and inhibition of return (IOR) for longer delays. SCZ, however, showed an apparent shift in the time course of cuing effects in the form of a delayed onset of IOR. Using a task of reflexive orienting, these results support findings of a delayed rather than an absent inhibitory process in medicated SCZ.

Nicotine, caffeine, alcohol and schizotypy

Abstract Schizophrenics are known to be heavy smokers. It has also been reported that in a normal population smoking is associated with higher scores on scales of schizotypy. The present study investigated the use of nicotine as related to scores on a positive symptoms scale of schizotypy. 285 undergraduate students at Rutgers University completed the Rust Inventory of Schizotypal Cognitions (RISC) in addition to a questionnaire regarding smoking habits, caffeine and alcohol use. Results showed a relationship between schizotypy and the use nicotine, and also the use of caffeine and alcohol. Use of the stimulants caffeine and nicotine were associated with higher RISC scores, whereas low stimulant users (nonsmoking, low caffeine users) scored the lowest on the administered scale of schizotypy. The effects of both stimulants were not additive, as demonstrated by a significant interaction between nicotine and caffeine use. The use of alcohol, a CNS depressant, showed the opposite relationship, with increasing alcohol use associated with lower RISC scores. The relationship between schizotypy and increased use of stimulants and decreased use of depressants is discussed.

Voluntary Spatial Attention has Different Effects on Voluntary and Reflexive Saccades

Although numerous studies have investigated the relationship between saccadic eye movements and spatial attention, one fundamental issue remains controversial. Some studies have suggested that spatial attention facilitates saccades, whereas others have claimed that eye movements are actually inhibited when spatial attention is engaged. However, these discrepancies may be because previous research has neglected to separate and specify the effects of attention for two distinct types of saccades, namely reflexive (stimulus-directed) and voluntary (antisaccades). The present study explored the effects of voluntary spatial attention on both voluntary and reflexive saccades. Results indicate that voluntary spatial attention has different effects on the two types of saccades. Antisaccades were always greatly facilitated following the engagement of spatial attention by symbolic cues (arrows) informing the subject where the upcoming saccade should be directed. Reflexive saccades showed little or no cueing effects and exhibited significant facilitation only when these cues were randomly intermixed with uncued trials. In addition, the present study tested the effects of fixation condition (gap, step, and overlap) on attentional modulation. Cueing effects did not vary due to fixation condition. Thus, voluntary spatial attention consistently showed different effects on voluntary and reflexive saccades, and there was no evidence in these studies that voluntary cues inhibit reflexive saccades, even in a gap paradigm.

Dissociating sensory and motor components of inhibition of return.

Two explanations for inhibition of return (IOR) have been proposed. The first is that IOR reflects inhibition of attentional processing at previously cued locations, resulting in altered sensory analysis. The second is that IOR reflects the inhibition of responses directed towards those previously cued locations. We used a variant of a double-saccade paradigm to dissociate these two proposed effects of IOR and attempted to reveal both effects within the context of a single experimental task. Subjects viewed a series of exogenous cues and then made a localization response to subsequent targets with either a target-directed saccade or a pointing response. Results were similar for both response modes. An important finding was that the pattern of IOR depended critically on how subjects reacted to the exogenous cues. Subjects either oriented to the cued locations (via saccades or pointing) prior to responding to the target (Respond), or passively viewed the cues before responding (Ignore). In the Respond condition, IOR was observed at the most recently cued position. Although this could be consistent with an altered sensory interpretation, it would also be consistent with a spatiotopic representation. In the Ignore condition, the sole inhibited location was not the most recently cued position, but the first cued position. This finding is surprising and in conflict with previous work with multiple exogenous cues. The data are discussed in relation to a number of prominent issues in the area of IOR and suggest important new constraints and boundary conditions.