Saccade-related Activity Research Articles

Functional specialization and distributed processing across marmoset lateral prefrontal subregions.

A prominent aspect of primate lateral prefrontal cortex organization is its division into several cytoarchitecturally distinct subregions. Neurophysiological investigations in macaques have provided evidence for the functional specialization of these subregions, but an understanding of the relative representational topography of sensory, social, and cognitive processes within them remains elusive. One explanatory factor is that evidence for functional specialization has been compiled largely from a patchwork of findings across studies, in many animals, and with considerable variation in stimulus sets and tasks. Here, we addressed this by leveraging the common marmoset (Callithrix jacchus) to carry out large-scale neurophysiological mapping of the lateral prefrontal cortex using high-density microelectrode arrays, and a diverse suite of test stimuli including faces, marmoset calls, and spatial working memory task. Task-modulated units and units responsive to visual and auditory stimuli were distributed throughout the lateral prefrontal cortex, while those with saccade-related activity or face-selective responses were restricted to 8aV, 8aD, 10, 46V, and 47. Neurons with contralateral visual receptive fields were limited to areas 8aV and 8aD. These data reveal a mixed pattern of functional specialization in the lateral prefrontal cortex, in which responses to some stimuli and tasks are distributed broadly across lateral prefrontal cortex subregions, while others are more limited in their representation.

Differential clustering of visual and choice- and saccade-related activity in macaque V3A and CIP.

Neurons in sensory and motor cortices tend to aggregate in clusters with similar functional properties. Within the primate dorsal ("where") pathway, an important interface between three-dimensional (3-D) visual processing and motor-related functions consists of two hierarchically organized areas: V3A and the caudal intraparietal (CIP) area. In these areas, 3-D visual information, choice-related activity, and saccade-related activity converge, often at the single-neuron level. Characterizing the clustering of functional properties in areas with mixed selectivity, such as these, may help reveal organizational principles that support sensorimotor transformations. Here we quantified the clustering of visual feature selectivity, choice-related activity, and saccade-related activity by performing correlational and parametric comparisons of the responses of well-isolated, simultaneously recorded neurons in macaque monkeys. Each functional domain showed statistically significant clustering in both areas. However, there were also domain-specific differences in the strength of clustering across the areas. Visual feature selectivity and saccade-related activity were more strongly clustered in V3A than in CIP. In contrast, choice-related activity was more strongly clustered in CIP than in V3A. These differences in clustering may reflect the areas' roles in sensorimotor processing. Stronger clustering of visual and saccade-related activity in V3A may reflect a greater role in within-domain processing, as opposed to cross-domain synthesis. In contrast, stronger clustering of choice-related activity in CIP may reflect a greater role in synthesizing information across functional domains to bridge perception and action.NEW & NOTEWORTHY The occipital and parietal cortices of macaque monkeys are bridged by hierarchically organized areas V3A and CIP. These areas support 3-D visual transformations, carry choice-related activity during 3-D perceptual tasks, and possess saccade-related activity. This study quantifies the functional clustering of neuronal response properties within V3A and CIP for each of these domains. The findings reveal domain-specific cross-area differences in clustering that may reflect the areas' roles in sensorimotor processing.

Mixed Selectivity Coding of Content-Temporal Detail by Dorsomedial Posterior Parietal Neurons.

The dorsomedial posterior parietal cortex (dmPPC) is part of a higher-cognition network implicated in elaborate processes underpinning memory formation, recollection, episode reconstruction, and temporal information processing. Neural coding for complex episodic processing is however under-documented. Here, we recorded extracellular neural activities from three male rhesus macaques (Macaca mulatta) and revealed a set of neural codes of "neuroethogram" in the primate parietal cortex. Analyzing neural responses in macaque dmPPC to naturalistic videos, we discovered several groups of neurons that are sensitive to different categories of ethogram items, low-level sensory features, and saccadic eye movement. We also discovered that the processing of category and feature information by these neurons is sustained by the accumulation of temporal information over a long timescale of up to 30 s, corroborating its reported long temporal receptive windows. We performed an additional behavioral experiment with additional two male rhesus macaques and found that saccade-related activities could not account for the mixed neuronal responses elicited by the video stimuli. We further observed monkeys' scan paths and gaze consistency are modulated by video content. Taken altogether, these neural findings explain how dmPPC weaves fabrics of ongoing experiences together in real time. The high dimensionality of neural representations should motivate us to shift the focus of attention from pure selectivity neurons to mixed selectivity neurons, especially in increasingly complex naturalistic task designs.

Parallel processing, hierarchical transformations, and sensorimotor associations along the 'where' pathway.

Visually guided behaviors require the brain to transform ambiguous retinal images into object-level spatial representations and implement sensorimotor transformations. These processes are supported by the dorsal 'where' pathway. However, the specific functional contributions of areas along this pathway remain elusive due in part to methodological differences across studies. We previously showed that macaque caudal intraparietal (CIP) area neurons possess robust 3D visual representations, carry choice- and saccade-related activity, and exhibit experience-dependent sensorimotor associations (Chang et al., 2020b). Here, we used a common experimental design to reveal parallel processing, hierarchical transformations, and the formation of sensorimotor associations along the 'where' pathway by extending the investigation to V3A, a major feedforward input to CIP. Higher-level 3D representations and choice-related activity were more prevalent in CIP than V3A. Both areas contained saccade-related activity that predicted the direction/timing of eye movements. Intriguingly, the time course of saccade-related activity in CIP aligned with the temporally integrated V3A output. Sensorimotor associations between 3D orientation and saccade direction preferences were stronger in CIP than V3A, and moderated by choice signals in both areas. Together, the results explicate parallel representations, hierarchical transformations, and functional associations of visual and saccade-related signals at a key juncture in the 'where' pathway.

Delayed Onset of Inhibition of Return in Visual Snow Syndrome.

Visual snow syndrome (VSS) is a complex, sensory processing disorder. We have previously shown that visual processing changes manifest in significantly faster eye movements toward a suddenly appearing visual stimulus and difficulty inhibiting an eye movement toward a non-target visual stimulus. We propose that these changes reflect poor attentional control and occur whether attention is directed exogenously by a suddenly appearing event, or endogenously as a function of manipulating expectation surrounding an upcoming event. Irrespective of how attention is captured, competing facilitatory and inhibitory processes prioritise sensory information that is important to us, filtering out that which is irrelevant. A well-known feature of this conflict is the alteration to behaviour that accompanies variation in the temporal relationship between competing sensory events that manipulate facilitatory and inhibitory processes. A classic example of this is the “Inhibition of Return” (IOR) phenomenon that describes the relative slowing of a response to a validly cued location compared to invalidly cued location with longer cue/target intervals. This study explored temporal changes in the allocation of attention using an ocular motor version of Posner's IOR paradigm, manipulating attention exogenously by varying the temporal relationship between a non-predictive visual cue and target stimulus. Forty participants with VSS (20 with migraine) and 20 controls participated. Saccades were generated to both validly cued and invalidly cued targets with 67, 150, 300, and 500 ms cue/target intervals. VSS participants demonstrated delayed onset of IOR. Unlike controls, who exhibited IOR with 300 and 500 ms cue/target intervals, VSS participants only exhibited IOR with 500 ms cue/target intervals. These findings provide further evidence that attention is impacted in VSS, manifesting in a distinct saccadic behavioural profile, and delayed onset of IOR. Whether IOR is perceived as the build-up of an inhibitory bias against returning attention to an already inspected location or a consequence of a stronger attentional orienting response elicited by the cue, our results are consistent with the proposal that in VSS, a shift of attention elicits a stronger increase in saccade-related activity than healthy controls. This work provides a more refined saccadic behavioural profile of VSS that can be interrogated further using sophisticated neuroimaging techniques and may, in combination with other saccadic markers, be used to monitor the efficacy of any future treatments.

Eye movement characteristics provide an objective measure of visual processing changes in patients with visual snow syndrome

Visual snow syndrome (VSS) is a poorly understood neurological disorder that features a range of disabling sensory changes. Visual processing changes revealed previously in VSS appear consistent with poor attentional control, specifically, with difficulty controlling environmentally driven shifts of attention. This study sought to confirm this proposal by determining whether these changes were similarly evident where attention is internally driven. Sixty seven VSS patients and 37 controls completed two saccade tasks: the endogenously cued saccade task and saccadic Simon task. The endogenously cued saccade task correctly (valid trial) or incorrectly (invalid trial) pre-cues a target location using a centrally presented arrow. VSS patients generated significantly shorter saccade latencies for valid trials (p = 0.03), resulting in a greater magnitude cue effect (p = 0.02), i.e. the difference in latency between valid and invalid trials. The saccadic Simon task presents a peripheral cue which may be spatially congruent or incongruent with the subsequent target location. Latencies on this task were comparable for VSS patients and controls, with a normal Simon effect, i.e. shorter latencies for saccades to targets spatially congruent with the preceding cue. On both tasks, VSS patients generated more erroneous saccades than controls towards non-target locations (Endogenously cued saccade task: p = 0.02, saccadic Simon task: p = 0.04). These results demonstrate that cued shifts of attention differentially affect saccade generation in VSS patients. We propose that these changes are not due to impairment of frontally-mediated inhibitory control, but to heightened saccade-related activity in visual regions. These results contribute to a VSS ocular motor signature that may provide clinical utility as well as an objective measure of dysfunction to facilitate future research.

The posterior parietal cortex contributes to visuomotor processing for saccades in blindsight macaques

Patients with damage to the primary visual cortex (V1) lose visual awareness, yet retain the ability to perform visuomotor tasks, which is called “blindsight.” To understand the neural mechanisms underlying this residual visuomotor function, we studied a non-human primate model of blindsight with a unilateral lesion of V1 using various oculomotor tasks. Functional brain imaging by positron emission tomography showed a significant change after V1 lesion in saccade-related visuomotor activity in the intraparietal sulcus area in the ipsi- and contralesional posterior parietal cortex. Single unit recordings in the lateral bank of the intraparietal sulcus (lbIPS) showed visual responses to targets in the contralateral visual field on both hemispheres. Injection of muscimol into the ipsi- or contralesional lbIPSs significantly impaired saccades to targets in the V1 lesion-affected visual field, differently from previous reports in intact animals. These results indicate that the bilateral lbIPSs contribute to visuomotor function in blindsight.

Eye position signals in the dorsal pulvinar during fixation and goal-directed saccades.

Sensorimotor cortical areas contain eye position information thought to ensure perceptual stability across saccades and underlie spatial transformations supporting goal-directed actions. One pathway by which eye position signals could be relayed to and across cortical areas is via the dorsal pulvinar. Several studies have demonstrated saccade-related activity in the dorsal pulvinar, and we have recently shown that many neurons exhibit postsaccadic spatial preference. In addition, dorsal pulvinar lesions lead to gaze-holding deficits expressed as nystagmus or ipsilesional gaze bias, prompting us to investigate the effects of eye position. We tested three starting eye positions (-15°, 0°, 15°) in monkeys performing a visually cued memory saccade task. We found two main types of gaze dependence. First, ~50% of neurons showed dependence on static gaze direction during initial and postsaccadic fixation, and might be signaling the position of the eyes in the orbit or coding foveal targets in a head/body/world-centered reference frame. The population-derived eye position signal lagged behind the saccade. Second, many neurons showed a combination of eye-centered and gaze-dependent modulation of visual, memory, and saccadic responses to a peripheral target. A small subset showed effects consistent with eye position-dependent gain modulation. Analysis of reference frames across task epochs from visual cue to postsaccadic fixation indicated a transition from predominantly eye-centered encoding to representation of final gaze or foveated locations in nonretinocentric coordinates. These results show that dorsal pulvinar neurons carry information about eye position, which could contribute to steady gaze during postural changes and to reference frame transformations for visually guided eye and limb movements.NEW & NOTEWORTHY Work on the pulvinar focused on eye-centered visuospatial representations, but position of the eyes in the orbit is also an important factor that needs to be taken into account during spatial orienting and goal-directed reaching. We show that dorsal pulvinar neurons are influenced by eye position. Gaze direction modulated ongoing firing during stable fixation, as well as visual and saccade responses to peripheral targets, suggesting involvement of the dorsal pulvinar in spatial coordinate transformations.

The fixation-related lambda response: Effects of saccade magnitude, spatial frequency, and ocular artifact removal.

Fixation-related potentials (FRPs) enable examination of electrophysiological signatures of visual perception under naturalistic conditions, providing a neural snapshot of the fixated scene. The most prominent FRP component, commonly referred to as the lambda response, is a large deflection over occipital electrodes (O1, Oz, O2) peaking 80-100 ms post fixation, reflecting afferent input to visual cortex. The lambda response is affected by bottom-up stimulus features and the size of the preceding saccade; however, prior research has not adequately controlled for these influences in free viewing paradigms. The current experiment (N = 16, 1 female) addresses these concerns by systematically manipulating spatial frequency in a free-viewing task requiring a range of saccade sizes. Given the close temporal proximity between saccade related activity and the onset of the lambda response, we evaluate how removing independent components (IC) associated with ocular motion artifacts affects lambda response amplitude. Our results indicate that removing ocular artifact ICs based on the covariance with gaze position did not significantly affect the amplitude of this occipital potential. Moreover, the results showed that spatial frequency and saccade magnitude each produce significant effects on lambda amplitude, where amplitude decreased with increasing spatial frequency and increased as a function of saccade size for small and medium-sized saccades. The amplitude differences between spatial frequencies were maintained across all saccade magnitudes suggesting these effects are produced from distinctly different and uncorrelated mechanisms. The current results will inform future analyses of the lambda potential in natural scenes where saccade magnitudes and spatial frequencies ultimately vary.

Neuronal Correlates of Serial Decision-Making in the Supplementary Eye Field.

Human behavior is influenced by serial decision-making: past decisions affect choices that set the context for selecting future options. A primate brain region that may be involved in linking decisions across time is the supplementary eye field (SEF), which, in addition to its well known visual responses and saccade-related activity, also signals the rules that govern flexible decisions and the outcomes of those decisions. Our hypotheses were that SEF neurons encode events during serial decision-making and link the sequential decisions with sustained activity. We recorded from neurons in the SEF of two rhesus monkeys (Macaca mulatta, one male, one female) that performed a serial decision-making task. The monkeys used saccades to select a rule that had to be applied later in the same trial to discriminate between visual stimuli. We found, first, that SEF neurons encoded the spatial parameters of saccades during rule selection but not during visual discrimination, suggesting a malleability to their movement-related tuning. Second, SEF activity linked the sequential decisions of rule selection and visual discrimination, but not continuously. Instead, rule-encoding activity appeared in a "just-in-time" manner before the visual discrimination. Third, SEF neurons encoded trial outcomes both prospectively, before decisions within a trial, and retrospectively, across multiple trials. The results thus identify neuronal correlates of rule selection and application in the SEF, including transient signals that link these sequential decisions. Its activity patterns suggest that the SEF participates in serial decision-making in a contextually dependent manner as part of a broader network.SIGNIFICANCE STATEMENT Much research has gone into studying the neurobiological basis of single, isolated decisions. An important next step is to understand how the brain links multiple decisions to generate a coherent stream of thought and behavior. We studied neural activity related to serial decision-making in an area of frontal cortex known as the supplementary eye field (SEF). Neural recordings were conducted in monkeys that performed a serial decision-making task in which they selected and applied rules. We found that SEF neurons convey signals for serial decision-making, including transient encoding of one decision at the time it is needed for the next one and longer-term representations of trial outcomes, suggesting that the region plays a role in continuity of cognition and behavior.

Neuronal Encoding of Self and Others\u2019 Head Rotation in the Macaque Dorsal Prefrontal Cortex

Following gaze is a crucial skill, in primates, for understanding where and at what others are looking, and often requires head rotation. The neural basis underlying head rotation are deemed to overlap with the parieto-frontal attention/gaze-shift network. Here, we show that a set of neurons in monkey’s Brodmann area 9/46dr (BA 9/46dr), which is involved in orienting processes and joint attention, becomes active during self head rotation and that the activity of these neurons cannot be accounted for by saccade-related activity (head-rotation neurons). Another set of BA 9/46dr neurons encodes head rotation performed by an observed agent facing the monkey (visually triggered neurons). Among these latter neurons, almost half exhibit the intriguing property of encoding both execution and observation of head rotation (mirror-like neurons). Finally, by means of neuronal tracing techniques, we showed that BA 9/46dr takes part into two distinct networks: a dorso/mesial network, playing a role in spatial head/gaze orientation, and a ventrolateral network, likely involved in processing social stimuli and mirroring others’ head. The overall results of this study provide a new, comprehensive picture of the role of BA 9/46dr in encoding self and others’ head rotation, likely playing a role in head-following behaviors.

Activity in the human superior colliculus relating to endogenous saccade preparation and execution.

In recent years a small number of studies have applied functional imaging techniques to investigate visual responses in the human superior colliculus (SC), but few have investigated its oculomotor functions. Here, in two experiments, we examined activity associated with endogenous saccade preparation. We used 3-T fMRI to record the hemodynamic activity in the SC while participants were either preparing or executing saccadic eye movements. Our results showed that not only executing a saccade (as previously shown) but also preparing a saccade produced an increase in the SC hemodynamic activity. The saccade-related activity was observed in the contralateral and to a lesser extent the ipsilateral SC. A second experiment further examined the contralateral mapping of saccade-related activity with a larger range of saccade amplitudes. Increased activity was again observed in both the contralateral and ipsilateral SC that was evident for large as well as small saccades. This suggests that the ipsilateral component of the increase in BOLD is not due simply to small-amplitude saccades producing bilateral activity in the foveal fixation zone. These studies provide the first evidence of presaccadic preparatory activity in the human SC and reveal that fMRI can detect activity consistent with that of buildup neurons found in the deeper layers of the SC in studies of nonhuman primates.

Effector specificity in macaque frontal and parietal cortex.

Single neurons in the frontal eye fields (FEFs) and lateral intraparietal area (LIP) of macaques are preferentially activated by saccade- versus reach-related processes. fMRI studies focusing on saccade- and reach-specific activity in human cortex, however, provided conflicting evidence for effector specificity. To gain further insights into effector preferences throughout monkey cortex using the same technique as in humans, we performed a mixed block/event-related fMRI experiment in macaques. Within single fMRI runs, monkeys alternated between a visually guided saccade task, a visually guided arm movement task, and a fixation-only task requiring no saccades or arm movements. The detection of a peripheral pop-out go cue initiating the required operant behavior and the identification of a target among distractors was identical in the arm and saccade tasks. We found saccade-related activity in parietal areas V6, V6A, LIP, and caudal intraparietal area and frontal areas FEF, 45a, 45b, and 46. Areas 45 and FEF even showed markedly decreased fMRI activity during arm movements relative to fixation only. Conversely, medial and anterior intraparietal areas (MIP and AIP), and parietal area PEip; somatosensory areas S1 and S2; and (pre)motor areas F1, F3, F5, and F6 showed increased arm movement-related activity. F1, F5, PEip, and somatosensory cortex also showed deactivations during saccades relative to fixation only. Control experiments showed that such deactivations in both operant-specific functional networks did not depend on training history or rapid task switching requiring active suppression of the unpreferred operant behavior. Therefore, although both tasks required divided attention to detect a pop-out go cue and target, two largely segregated and mainly effector-driven cortical networks were activated.

Neural correlates of target selection for reaching movements in superior colliculus.

We recently demonstrated that inactivation of the primate superior colliculus (SC) causes a deficit in target selection for arm-reaching movements when the reach target is located in the inactivated field (Song JH, Rafal RD, McPeek RM. Proc Natl Acad Sci USA 108: E1433-E1440, 2011). This is consistent with the notion that the SC is part of a general-purpose target selection network beyond eye movements. To understand better the role of SC activity in reach target selection, we examined how individual SC neurons in the intermediate layers discriminate a reach target from distractors. Monkeys reached to touch a color oddball target among distractors while maintaining fixation. We found that many SC neurons robustly discriminate the goal of the reaching movement before the onset of the reach even though no saccade is made. To identify these cells in the context of conventional SC cell classification schemes, we also recorded visual, delay-period, and saccade-related responses in a delayed saccade task. On average, SC cells that discriminated the reach target from distractors showed significantly higher visual and delay-period activity than nondiscriminating cells, but there was no significant difference in saccade-related activity. Whereas a majority of SC neurons that discriminated the reach target showed significant delay-period activity, all nondiscriminating cells lacked such activity. We also found that some cells without delay-period activity did discriminate the reach target from distractors. We conclude that the majority of intermediate-layer SC cells discriminate a reach target from distractors, consistent with the idea that the SC contains a priority map used for effector-independent target selection.

Saccade-related activity in the prefrontal cortex: its role in eye movement control and cognitive functions.

Prefrontal neurons exhibit saccade-related activity and pre-saccadic memory-related activity often encodes the directions of forthcoming eye movements, in line with demonstrated prefrontal contribution to flexible control of voluntary eye movements. However, many prefrontal neurons exhibit post-saccadic activity that is initiated well after the initiation of eye movement. Although post-saccadic activity has been observed in the frontal eye field, this activity is thought to be a corollary discharge from oculomotor centers, because this activity shows no directional tuning and is observed whenever the monkeys perform eye movements regardless of goal-directed or not. However, prefrontal post-saccadic activities exhibit directional tunings similar as pre-saccadic activities and show context dependency, such that post-saccadic activity is observed only when monkeys perform goal-directed saccades. Context-dependency of prefrontal post-saccadic activity suggests that this activity is not a result of corollary signals from oculomotor centers, but contributes to other functions of the prefrontal cortex. One function might be the termination of memory-related activity after a behavioral response is done. This is supported by the observation that the termination of memory-related activity coincides with the initiation of post-saccadic activity in population analyses of prefrontal activities. The termination of memory-related activity at the end of the trial ensures that the subjects can prepare to receive new and updated information. Another function might be the monitoring of behavioral performance, since the termination of memory-related activity by post-saccadic activity could be associated with informing the correctness of the response and the termination of the trial. However, further studies are needed to examine the characteristics of saccade-related activities in the prefrontal cortex and their functions in eye movement control and a variety of cognitive functions.

Fixational saccade-related activity of pedunculopontine tegmental nucleus neurons in behaving monkeys.

Fixational saccades are small, involuntary eye movements that occur during attempted visual fixation. Recent studies suggested that several cognitive processes affect the occurrence probability of fixational saccades. Thus, there might be an interaction between fixational saccade-related motor signals and cognitive signals. The pedunculopontine tegmental nucleus (PPTN) in the brainstem has anatomical connections with numerous saccade-related and limbic areas. Previously, we reported that a group of PPTN neurons showed transient phasic bursts or a pause in activity during large visually guided and spontaneous saccades, and also showed sustained tonic changes in activity with task context. We hypothesised that single PPTN neurons would relay both fixational saccade-related and task context-related signals, and might function as an interface between the motor and limbic systems. We recorded the activity of PPTN neurons in behaving monkeys during a reward-biased task, and analysed neuronal activity for small fixational saccades during visual fixation, and compared it with the activity for large visually guided targeting saccades and large spontaneous saccades during intertrial intervals. A population of PPTN neurons exhibited a fixational saccade-related phasic increase in activity, and the majority of them also showed activity modulation with large targeting saccades. In addition, a group of these neurons showed a task-related tonic increase in activity during the fixation period, and half of them relayed the saccade signal only when the neuron exhibited higher tonic activity during the task execution period. Thus, fixational saccade-related signals of PPTN neurons overlap with tonic task-related signals, and might contribute to the cognitive modulation of fixational saccades.

Anatomical evidence that the superior colliculus controls saccades through central mesencephalic reticular formation gating of omnipause neuron activity.

Omnipause neurons (OPNs) within the nucleus raphe interpositus (RIP) help gate the transition between fixation and saccadic eye movements by monosynaptically suppressing activity in premotor burst neurons during fixation, and releasing them during saccades. Premotor neuron activity is initiated by excitatory input from the superior colliculus (SC), but how the tectum's saccade-related activity turns off OPNs is not known. Since the central mesencephalic reticular formation (cMRF) is a major SC target, we explored whether this nucleus has the appropriate connections to support tectal gating of OPN activity. In dual-tracer experiments undertaken in macaque monkeys (Macaca fascicularis), cMRF neurons labeled retrogradely from injections into RIP had numerous anterogradely labeled terminals closely associated with them following SC injections. This suggested the presence of an SC-cMRF-RIP pathway. Furthermore, anterograde tracers injected into the cMRF of other macaques labeled axonal terminals in RIP, confirming this cMRF projection. To determine whether the cMRF projections gate OPN activity, postembedding electron microscopic immunochemistry was performed on anterogradely labeled cMRF terminals with antibody to GABA or glycine. Of the terminals analyzed, 51.4% were GABA positive, 35.5% were GABA negative, and most contacted glycinergic cells. In summary, a trans-cMRF pathway connecting the SC to the RIP is present. This pathway contains inhibitory elements that could help gate omnipause activity and allow other tectal drives to induce the bursts of firing in premotor neurons that are necessary for saccades. The non-GABAergic cMRF terminals may derive from fixation units in the cMRF.

Macaque Dorsolateral Prefrontal Cortex Does not Suppress Saccade-Related Activity in the Superior Colliculus

Of the many functions ascribed to the dorsolateral prefrontal cortex (DLPFC), the ability to override automatic stimulus-driven behavior is one of the most prominent. This ability has been investigated extensively with the antisaccade task, which requires suppression of saccades toward suddenly appearing visual stimuli. Convergent lines of evidence have supported a model in which the DLPFC suppresses unwanted saccades by inhibiting saccade-related activity in the ipsilateral superior colliculus (SC), a midbrain oculomotor structure. Here, we carried out a direct test of this inhibitory model using unilateral cryogenic deactivation of the DLPFC within the caudal principal sulcus (cPS) and simultaneous single-neuron recording of SC saccade-related neurons in monkeys performing saccades and antisaccades. Contrary to the inhibition model, which predicts that attenuation of inhibition effected by unilateral cPS deactivation should result in activity increases in ipsilateral and decreases in contralateral SC, we observed a delayed onset of saccade-related activity in the ipsilateral SC, and activity increases in the contralateral SC. These effects were mirrored by increased error rates of ipsiversive antisaccades, and reaction times of contraversive saccades. These data challenge the inhibitory model and suggest instead that the primary influence of the DLPFC on the SC is excitatory.

The parietal cortex and saccade planning: lessons from human lesion studies.

The parietal cortex is a critical interface for attention and integration of multiple sensory signals that can be used for the implementation of motor plans. Many neurons in this region exhibit strong attention-, reach-, grasp- or saccade-related activity. Here, we review human lesion studies supporting the critical role of the parietal cortex in saccade planning. Studies of patients with unilateral parietal damage and spatial neglect reveal characteristic spatially lateralized deficits of saccade programming when multiple stimuli compete for attention. However, these patients also show bilateral impairments of saccade initiation and control that are difficult to explain in the context of their lateralized deficits of visual attention. These findings are reminiscent of the deficits of oculomotor control observed in patients with Bálint's syndrome consecutive to bilateral parietal damage. We propose that some oculomotor deficits following parietal damage are compatible with a decisive role of the parietal cortex in saccade planning under conditions of sensory competition, while other deficits reflect disinhibition of low-level structures of the oculomotor network in the absence of top-down parietal modulation.

Cross-frequency phase synchrony around the saccade period as a correlate of perceiver's internal state.

In active vision, eye-movements depend on perceivers' internal state. We investigated peri-fixation brain activity for internal state-specific tagging. Human participants performed a task, in which a visual object was presented for identification in lateral visual field, to which they moved their eyes as soon as possible from a central fixation point. Next, a phrase appeared in the same location; the phrase could either be an easy or hard question about the object, answered by pressing one of two alternative response buttons, or it could be an instruction to simply press one of these two buttons. Depending on whether these messages were blocked or randomly mixed, one of two different internal states was induced: either the task was known in advance or it wasn't. Eye movements and electroencephalogram (EEG) were recorded simultaneously during task performance. Using eye-event-time-locked averaging and independent component analysis, saccade- and fixation-related components were identified. Coss-frequency phase-synchrony was observed between the alpha/beta1 ranges of fixation-related and beta2/gamma1 ranges of saccade-related activity 50 ms prior to fixation onset in the mixed-phrase condition only. We interpreted this result as evidence for internal state-specific tagging.