Comparison of memory- and visually guided saccades using event-related fMRI.
M. R. G. Brown, J. F. X. DeSouza, H. C. Goltz, K. Ford, R. S. Menon, M. A. Goodale, and S. Everling
Previous functional imaging studies have shown an increased hemodynamic signal in several cortical areas when subjects perform memory-guided saccades than that when they perform visually guided saccades using blocked trial designs. It is unknown, however, whether this difference results from sensory processes associated with stimulus presentation, from processes occurring during the delay period before saccade generation, or from an increased motor signal for memory-guided saccades. We conducted fMRI using an event-related paradigm that separated stimulus-related, delay-related, and saccade-related activity. Subjects initially fixated a central cross, whose color indicated whether the trial was a memory- or a visually guided trial. A peripheral stimulus was then flashed at one of 4 possible locations. On memory-guided trials, subjects had to remember this location for the subsequent saccade, whereas the stimulus was a distractor on visually guided trials. Fixation cross disappearance after a delay period was the signal either to generate a memory-guided saccade or to look at a visual stimulus that was flashed on visually guided trials. We found slightly greater stimulus-related activation for visually guided trials in 3 right prefrontal regions and right rostral intraparietal sulcus (IPS). Memory-guided trials evoked greater delay-related activity in right posterior inferior frontal gyrus, right medial frontal eye field, bilateral supplementary eye field, right rostral IPS, and right ventral IPS but not in middle frontal gyrus. Right precentral gyrus and right rostral IPS exhibited greater saccade-related activation on memory-guided trials. We conclude that activation differences revealed by previous blocked experiments have different sources in different areas and that cortical saccade regions exhibit delay-related activation differences.
Effect of reversible inactivation of macaque lateral intraparietal area on visual and memory saccades.
C. S. Li, P. Mazzoni, and R. A. Andersen
Previous studies from our laboratory identified a parietal eye field in the primate lateral intraparietal sulcus, the lateral intraparietal area (area LIP). Here we further explore the role of area LIP in processing saccadic eye movements by observing the effects of reversible inactivation of this area. One to 2 microl of muscimol (8 mg/ml) were injected at locations where saccade-related activities were recorded for each lesion experiment. After the muscimol injection we observed in two macaque monkeys consistent effects on both the metrics and dynamics of saccadic eye movements at many injection sites. These effects usually took place within 10-30 min and disappeared after 5-6 h in most cases and certainly when tested the next day. After muscimol injection memory saccades directed toward the contralesional and upper space became hypometric, and in one monkey those to the ipsilesional space were slightly but significantly hypermetric. In some cases, the scatter of the end points of memory saccades was also increased. On the other hand, the metrics of visual saccades remained relatively intact. Latency for both visual and memory saccades toward the contralesional space was increased and in many cases displayed a higher variance after muscimol lesion. At many injection sites we also observed an increase of latency for visual and memory saccades toward the upper space. The peak velocities for memory saccades toward the contralesional space were decreased after muscimol injection. The peak velocities of visual saccades were not significantly different from those of the controls. The duration of saccadic eye movements either to the ipsilesional or contralesional space remained relatively the same for both visual and memory saccades. Overall these results demonstrated that we were able to selectively inactivate area LIP and observe effects on saccadic eye movements. Together with our previous recording studies these results futher support the view that area LIP plays a direct role in processing incoming sensory information to program saccadic eye movements. The results are consistent with our unit recording data and microstimulation studies, which suggest that area LIP represents contralateral space and also has a bias for the upper visual field.
Dissociation of spatial attention and saccade preparation.
C. Juan, S. M. Shorter-Jacobi, and J. D. Schall
Proc Natl Acad Sci U S A
The goal of this experiment was to determine whether the allocation of attention necessarily requires saccade preparation. To dissociate the focus of attention from the endpoint of a saccade, macaque monkeys were trained to perform visual search for a uniquely colored rectangle and shift gaze either toward or opposite this color singleton according to its orientation. A vertical singleton cued a prosaccade, a horizontal singleton, an antisaccade. Saccade preparation was probed by measuring the direction of saccades evoked by intracortical microstimulation of the frontal eye fields at variable times after presentation of the search array. Eye movements evoked on prosaccade trials deviated progressively toward the singleton that was also the endpoint of the correct eye movement. However, eye movements evoked on antisaccade trials never deviated toward the singleton but only progressively toward the location opposite the singleton. This occurred even though previous work showed that on antisaccade trials most neurons in frontal eye fields initially select the singleton while attention is allocated to distinguish its shape. Thus, sensorimotor structures can covertly orient attention without preparing a saccade.
Microstimulation of the frontal eye field and its effects on covert spatial attention.
T. Moore and M. Fallah
Many studies have established that the strength of visual perception and the strength of visual representations within visual cortex vary according to the focus of covert spatial attention. While it is clear that attention can modulate visual signals, the source of this modulation remains unknown. We have examined the possibility that saccade related mechanisms provide a source of spatial attention by studying the effects of electrical microstimulation of the frontal eye fields (FEF) on spatial attention. Monkeys performed a task in which they had to detect luminance changes of a peripheral target while ignoring a flashing distracter. The target luminance change could be preceded by stimulation of the FEF at current levels below that which evoked saccadic eye movements. We found that when the target change was preceded by stimulation of FEF, the monkey could detect smaller changes in target luminance. The increased sensitivity to the target change only occurred when the target was placed in the part of the visual field represented by neurons at the stimulation site. The magnitude of improvement depended on the temporal asynchrony of the stimulation onset and the target event. No significant effect of stimulation was observed when long intervals (>300 ms) between stimulation and the target event were used, and the magnitude of the increased sensitivity decreased systematically with increasing asynchrony. At the shortest asynchrony, FEF stimulation temporally overlapped the target event and the magnitude of the improvement was comparable to that of removing the distracter from the task. These results demonstrate that transient, but potent improvements in the deployment of covert spatial attention can be obtained by microstimulation of FEF sites from which saccadic eye movements are also evoked.
Visuomotor origins of covert spatial attention.
T. Moore, K. M. Armstrong, and M. Fallah
Covert spatial attention produces biases in perceptual performance and neural processing of behaviorally relevant stimuli in the absence of overt orienting movements. The neural mechanism that gives rise to these effects is poorly understood. This paper surveys past evidence of a relationship between oculomotor control and visual spatial attention and more recent evidence of a causal link between the control of saccadic eye movements by frontal cortex and covert visual selection. Both suggest that the mechanism of covert spatial attention emerges as a consequence of the reciprocal interactions between neural circuits primarily involved in specifying the visual properties of potential targets and those involved in specifying the movements needed to fixate them.
Electrical microstimulation of primate posterior parietal cortex initiates orienting and alerting components of covert attention.
E. B. Cutrell and R. T. Marrocco
Exp Brain Res
The posterior parietal cortex (PPC) is implicated in the control of visuospatial orienting, including both overt saccadic eye movements and covert shifts of attention (i.e., attention to a location other than at visual fixation). Some studies have suggested that the attentional system is part of the premotor processing in the brain, while others suggest they are separate. Here, we test how the PPC controls covert attention shifts in the absence of executed eye movements. Electrical microstimulation was applied to the right PPC while monkeys performed a spatial, cued target detection task, in which they were not allowed to move their gaze. At high currents, contralateral saccades were evoked. With currents below the thresholds for eliciting saccades, microstimulation produced a purely attentional shift (as indexed by decreased target reaction time) when a cue and target were presented in the contralateral visual field. This suggests that microstimulation can move attention specifically in the absence of any overt movements of the eyes or limbs. In addition, there was a reduction in reaction times in trials that did not evoke attentional orienting, suggesting a more general alerting effect of microstimulation These data provide direct evidence that the PPC may be a source of both attentional modulation of neuronal responses and saccadic eye movements to peripheral visual stimuli.
Change in motor plan, without a change in the spatial locus of attention, modulates activity in posterior parietal cortex.
L. H. Snyder, A. P. Batista, and R. A. Andersen
The lateral intraparietal area (LIP) of macaque monkey, and a parietal reach region (PRR) medial and posterior to LIP, code the intention to make visually guided eye and arm movements, respectively. We studied the effect of changing the motor plan, without changing the locus of attention, on single neurons in these two areas. A central target was fixated while one or two sequential flashes occurred in the periphery. The first appeared either within the response field of the neuron being recorded or else on the opposite side of the fixation point. Animals planned a saccade (red flash) or reach (green flash) to the flash location. In some trials, a second flash 750 ms later could change the motor plan but never shifted attention: second flashes always occurred at the same location as the preceding first flash. Responses in LIP were larger when a saccade was instructed (n = 20 cells), whereas responses in PRR were larger when a reach was instructed (n = 17). This motor preference was observed for both first flashes and second flashes. In addition, the response to a second flash depended on whether it affirmed or countermanded the first flash; second flash responses were diminished only in the former case. Control experiments indicated that this differential effect was not due to stimulus novelty. These findings support a role for posterior parietal cortex in coding specific motor intention and are consistent with a possible role in the nonspatial shifting of motor intention.
Separate body- and world-referenced representations of visual space in parietal cortex.
L. H. Snyder, K. L. Grieve, P. Brotchie, and R. A. Andersen
In order to direct a movement towards a visual stimulus, visual spatial information must be combined with postural information. For example, directing gaze (eye plus head) towards a visible target requires the combination of retinal image location with eye and head position to determine the location of the target relative to the body. Similarly, world-referenced postural information is required to determine where something lies in the world. Posterior parietal neurons recorded in monkeys combine visual information with eye and head position. A population of such cells could make up a distributed representation of target location in an extraretinal frame of reference. However, previous studies have not distinguished between world-referenced and body-referenced signals. Here we report that modulations of visual signals (gain fields) in two adjacent cortical fields, LIP and 7a, are referenced to the body and to the world, respectively. This segregation of spatial information is consistent with a streaming of information, with one path carrying body-referenced information for the control of gaze, and the other carrying world-referenced information for navigation and other tasks that require an absolute frame of reference.
Attentional processes link perception and action.
S. J. Anderson, N. Yamagishi, and V. Karavia
Proc Biol Sci
Behavioural studies on normal and brain-damaged individuals provide convincing evidence that the perception of objects results in the generation of both visual and motor signals in the brain, irrespective of whether or not there is an intention to act upon the object. In this paper we sought to determine the basis of the motor signals generated by visual objects. By examining how the properties of an object affect an observer's reaction time for judging its orientation, we provide evidence to indicate that directed visual attention is responsible for the automatic generation of motor signals associated with the spatial characteristics of perceived objects.
Neural coding of "attention for action" and "response selection"in primate anterior cingulate cortex.
Y. Isomura, Y. Ito, T. Akazawa, A. Nambu, and M. Takada
Noninvasive imaging techniques showed that the anterior cingulate cortex is related to higher-order cognitive and motor-related functions in humans. To elucidate the cellular mechanism of such cingulate functions, single-unit activity was recorded from three cingulate motor areas of macaque monkeys performing delayed conditional Go/No-go discrimination tasks using spatial (location) and nonspatial (color) visual cues. Unlike prefrontal neurons, only a few neurons coded the visual information on individual features (e.g., "left" or "red") in all of the rostral (CMAr), dorsal (CMAd), and ventral (CMAv) cingulate motor areas. Instead, many neurons in the CMAr exhibited the attention-like activity anticipating the second (conditioned) visual cues, with the specificity to visual category ("location" or "color"). In addition, there were a number of CMAr neurons specific to motor response (Go or No-go) in relation to the second visual cues. Some of the visual category-specific neurons in the CMAr further displayed the motor response-specific activity. On the other hand, many of the task-related CMAd and CMAv neurons seemed to be implicated directly in motor functions, such as preparation and execution of movements in Go trials. The present results suggest that the CMAr neurons may participate in cognitive and motor functions of "attention for action" and "response selection" for an appropriate action according to an intention, whereas the CMAd and CMAv neurons may be involved in "motor preparation and execution".
Maintenance of spatial and motor codes during oculomotor delayed response tasks.
C. E. Curtis, V. Y. Rao, and M. D'Esposito
The most compelling neural evidence for working memory is persistent neuronal activity bridging past sensory cues and their contingent future motor acts. This observation, however, does not answer what is actually being remembered or coded for by this activity. To address this fundamental issue, we imaged the human brain during maintenance of spatial locations and varied whether the memory-guided saccade was selected before or after the delay. An oculomotor delayed matching-to-sample task (match) was used to measure maintained motor intention because the direction of the forthcoming saccade was known throughout the delay. We used a nonmatching-to-sample task (nonmatch) in which the saccade was unpredictable to measure maintained spatial attention. Oculomotor areas were more active during match delays, and posterior parietal cortex and inferior frontal cortex were more active during nonmatch delays. Additionally, the fidelity of the memory was predicted by the delay-period activity of the frontal eye fields; the magnitude of delay-period activity correlated with the accuracy of the memory-guided saccade. Experimentally controlling response selection allowed us to functionally separate nodes of a network of frontal and parietal areas that usually coactivate in studies of working memory. We propose that different nodes in this network maintain different representational codes, motor and spatial. Which code is being represented by sustained neural activity is biased by when in the transformation from perception to action the response can be selected.
Attention to intention.
H. C. Lau, R. D. Rogers, P. Haggard, and R. E. Passingham
Intention is central to the concept of voluntary action. Using functional magnetic resonance imaging, we compared conditions in which participants made self-paced actions and attended either to their intention to move or to the actual movement. When they attended to their intention rather than their movement, there was an enhancement of activity in the pre-supplementary motor area (pre-SMA). We also found activations in the right dorsal prefrontal cortex and left intraparietal cortex. Prefrontal activity, but not parietal activity, was more strongly coupled with activity in the pre-SMA. We conclude that activity in the pre-SMA reflects the representation of intention.
High gamma frequency oscillatory activity dissociates attention from intention in the human premotor cortex.
A. Brovelli, J. Lachaux, P. Kahane, and D. Boussaoud
The premotor cortex is well known for its role in motor planning. In addition, recent studies have shown that it is also involved in nonmotor functions such as attention and memory, a notion derived from both animal neurophysiology and human functional imaging. The present study is an attempt to bridge the gap between these experimental techniques in the human brain, using a task initially designed to dissociate attention from intention in the monkey, and recently adapted for a functional magnetic resonance imaging (fMRI) study [Simon, S.R., Meunier, M., Piettre, L., Berardi, A.M., Segebarth, C.M., Boussaoud, D. (2002). Spatial attention and memory versus motor preparation: premotor cortex involvement as revealed by fMRI. J. Neurophysiol., 88, 2047-57]. Intracranial EEG was recorded from the cortical regions preferentially active in the spatial attention and/or working memory task and those involved in motor intention. The results show that, among the different intracranial EEG responses, only the high gamma frequency (60-200 Hz) oscillatory activity both dissociates attention/memory from motor intention and spatially colocalizes with the fMRI-identified premotor substrates of these two functions. This finding provides electrophysiological confirmation that the human premotor cortex is involved in spatial attention and/or working memory. Additionally, it provides timely support to the idea that high gamma frequency oscillations are involved in the cascade of neural processes underlying the hemodynamic responses measured with fMRI [Logothetis, N.K., Pauls, J., Augath, M., Trinath, T. and Oeltermann, A. (2001). Neurophysiological investigation of the basis of the fMRI signal. Nature, 412, 150-7], and suggests a functional selectivity of the gamma oscillations that could be critical for future EEG investigations, whether experimental or clinical.
Functional-anatomic correlates of memory retrieval that suggest nontraditional processing roles for multiple distinct regions within posterior parietal cortex.
B. J. Shannon and R. L. Buckner
Current theories of posterior parietal cortex (PPC) function emphasize space-based attention and motor intention. Imaging studies of long-term memory have demonstrated PPC activation during successful memory retrieval. Here, we explored the relationship between memory processes and classical notions of PPC function. Study 1 investigated old-new recognition using picture and sound stimuli to test whether PPC memory effects were dependent on visuospatial attention. A region lateral to the intraparietal sulcus [inferior parietal lobule complex (IPLC)] and two regions in the medial PPC [precuneus complex (PCC) and posterior cingulate/retrosplenial cortex (pC/Rsp)] showed strong retrieval success effects for both picture and sound stimuli. Study 2 explored a recognition task with varied response contingencies to investigate whether these retrieval success effects are dependent on motor intentions. In one condition, subjects responded to both old and new items. In two other conditions, subjects responded only to old or only to new items. IPLC, PCC, and pC/Rsp continued to show retrieval success effects with similar magnitudes for all response contingencies, including a condition in which no responses were made to old items. In a third study, IPLC and PCC activity was modulated at retrieval based on levels of processing at study, suggesting sensitivity to memory demands. These studies demonstrate that retrieval success effects in lateral and medial PPC regions are not affected by manipulations predicted by classical theories of PPC function but can be modulated by memory-related manipulations. PPC regions thus have prominent response properties associated with memory, which may arise through interactions with medial temporal cortex.
Covert manual response preparation triggers attentional shifts: ERP evidence for the premotor theory of attention.
M. Eimer, B. Forster, J. Van Velzen, and G. Prabhu
The premotor theory of attention claims that the preparation of goal-directed action and shifts of attention are closely linked, because they are controlled by shared sensorymotor mechanisms. Until now, support for this theory has come primarily from studies demonstrating links between saccade programming and attention shifts. The present event-related brain potential (ERP) study demonstrated that attentional orienting processes are also elicited during the covert preparation of unimanual responses. ERPs were recorded in the interval between a visual response-hand selection cue and a subsequent visual Go/Nogo signal when participants prepared to lift their left or right index finger. Lateralised ERP components elicited during response preparation were very similar to components previously observed during instructed endogenous attention shifts, indicating that analogous attentional orienting processes are activated in both cases. Somatosensory ERP components (P90, N140) were enhanced when task-irrelevant tactile probes were delivered during response preparation to the hand involved in an anticipated response, even when probes were presented well in advance of response execution. These results suggest that attentional shifts are triggered during unimanual response preparation, as predicted by the premotor theory. This link between manual response programming and attention is consistent with the hypothesis that common mechanisms are involved in the control of attention and action.
Frontoparietal control of spatial attention and motor intention in human EEG.
P. Praamstra, L. Boutsen, and G. W. Humphreys
Relations between spatial attention and motor intention were investigated by means of an EEG potential elicited by shifting attention to a location in space as well as by the selection of a hand for responding. High-density recordings traced this potential to a common frontoparietal network activated by attentional orienting and by response selection. Within this network, parietal and frontal cortex were activated sequentially, followed by an anterior-to-posterior migration of activity culminating in the lateral occipital cortex. Based on temporal and polarity information provided by EEG, we hypothesize that the frontoparietal activation, evoked by directional information, updates a task-defined preparatory state by deselecting or inhibiting the behavioral option competing with the cued response side or the cued direction of attention. These results from human EEG demonstrate a direct EEG manifestation of the frontoparietal attention network previously identified in functional imaging. EEG reveals the time-course of activation within this network and elucidates the generation and function of associated directing-attention EEG potentials. The results emphasize transient activation and a decision-related function of the frontoparietal attention network, contrasting with the sustained preparatory activation that is commonly inferred from neuroimaging.
The selection of intended actions and the observation of others' actions: a time-resolved fMRI study.
R. Cunnington, C. Windischberger, S. Robinson, and E. Moser
Whenever we plan, imagine, or observe an action, the motor systems that would be involved in preparing and executing that action are similarly engaged. The way in which such common motor activation is formed, however, is likely to differ depending on whether it arises from our own intentional selection of action or from the observation of another's action. In this study, we use time-resolved event-related functional MRI to tease apart neural processes specifically related to the processing of observed actions, the selection of our own intended actions, the preparation for movement, and motor response execution. Participants observed a finger gesture movement or a cue indicating they should select their own finger gesture to perform, followed by a 5-s delay period; participants then performed the observed or self-selected action. During the preparation and readiness for action, prior to initiation, we found activation in a common network of higher motor areas, including dorsal and ventral premotor areas and the pre-supplementary motor area (pre-SMA); the more caudal SMA showed greater activation during movement execution. Importantly, the route to this common motor activation differed depending on whether participants freely selected the actions to perform or whether they observed the actions performed by another person. Observation of action specifically involved activation of inferior and superior parietal regions, reflecting involvement of the dorsal visual pathway in visuomotor processing required for planning the action. In contrast, the selection of action specifically involved the dorsal lateral prefrontal and anterior cingulate cortex, reflecting the role of these prefrontal areas in attentional selection and guiding the selection of responses.
Movement intention is better predicted than attention in the posterior parietal cortex.
R. Quian Quiroga, L. H. Snyder, A. P. Batista, H. Cui, and R. A. Andersen
We decoded on a trial-by-trial basis the location of visual targets, as a marker of the locus of attention, and intentions to reach and to saccade in different directions using the activity of neurons in the posterior parietal cortex of two monkeys. Predictions of target locations were significantly worse than predictions of movement plans for the same target locations. Moreover, neural signals in the parietal reach region (PRR) gave better predictions of reaches than saccades, whereas signals in the lateral intraparietal area (LIP) gave better predictions of saccades than reaches. Taking together the activity of both areas, the prediction of either movement in all directions became nearly perfect. These results cannot be explained in terms of an attention effect and support the idea of two segregated populations in the posterior parietal cortex, PRR and LIP, that are involved in different movement plans.
Topographic organization for delayed saccades in human posterior parietal cortex.
D. Schluppeck, P. Glimcher, and D. J. Heeger
Posterior parietal cortex (PPC) is thought to play a critical role in decision making, sensory attention, motor intention, and/or working memory. Research on the PPC in non-human primates has focused on the lateral intraparietal area (LIP) in the intraparietal sulcus (IPS). Neurons in LIP respond after the onset of visual targets, just before saccades to those targets, and during the delay period in between. To study the function of posterior parietal cortex in humans, it will be crucial to have a routine and reliable method for localizing specific parietal areas in individual subjects. Here, we show that human PPC contains at least two topographically organized regions, which are candidates for the human homologue of LIP. We mapped the topographic organization of human PPC for delayed (memory guided) saccades using fMRI. Subjects were instructed to fixate centrally while a peripheral target was briefly presented. After a further 3-s delay, subjects made a saccade to the remembered target location followed by a saccade back to fixation and a 1-s inter-trial interval. Targets appeared at successive locations "around the clock" (same eccentricity, approximately 30 degrees angular steps), to produce a traveling wave of activity in areas that are topographically organized. PPC exhibited topographic organization for delayed saccades. We defined two areas in each hemisphere that contained topographic maps of the contra-lateral visual field. These two areas were immediately rostral to V7 as defined by standard retinotopic mapping. The two areas were separated from each other and from V7 by reversals in visual field orientation. However, we leave open the possibility that these two areas will be further subdivided in future studies. Our results demonstrate that topographic maps tile the cortex continuously from V1 well into PPC.
Parietal mechanisms of target representation.
Curr Opin Neurobiol
Recent single-neuron recordings show that representation of the external environment in the parietal lobe is highly selective for objects that are immediately relevant to behavior. Parietal neurons change their selectivity in accordance to immediate behavioral needs, integrate evidence about behavioral relevance from multiple sources, and appear to actively participate in the selection of potential behavioral targets. The selective parietal representations may represent a general-purpose attentional mechanism that can simultaneously specify targets for exploratory movements and for perception.
Integration of visuospatial and effector information during symbolically cued limb movements in monkey lateral intraparietal area.
J. Oristaglio, D. M. Schneider, P. F. Balan, and J. Gottlieb
Natural behavior requires close but flexible coordination between attention, defined as selection for perception, and action. In recent years a distributed network including the lateral intraparietal area (LIP) has been implicated in visuospatial selection for attention and rapid eye movements (saccades), but the relation between the attentional and motor functions of this area remains unclear. Here we tested LIP neurons in a task that involved not an ocular but a manual operant response. Monkeys viewed a display containing one cue and several distractors and reported the orientation of the cue (right- or left-facing) by releasing one of two bars grasped, respectively, with the right or left hand. The movement in this task thus was associated with (cued by), but not directed toward, the visual stimulus. A large majority of neurons responded more when the cue rather than when a distractor was in their receptive field, suggesting that they contribute to the attentional selection of the cue. A fraction of these neurons also was modulated by limb release, thus simultaneously encoding cue location and the active limb. The results suggest that the LIP links behaviorally relevant visual information with motor variables relevant for solving a task in a wide range of circumstances involving goal-directed or symbolically cued movements and eye as well as limb movements. A central function of the LIP may be to coordinate visual and motor selection during a wide variety of behaviors.
Distribution of activity across the monkey cerebral cortical surface, thalamus and midbrain during rapid, visually guided saccades.
J. T. Baker, G. H. Patel, M. Corbetta, and L. H. Snyder
To examine the distribution of visual and oculomotor activity across the macaque brain, we performed functional magnetic resonance imaging (fMRI) on awake, behaving monkeys trained to perform visually guided saccades. Two subjects alternated between periods of making saccades and central fixations while blood oxygen level dependent (BOLD) images were collected [3 T, (1.5 mm)3 spatial resolution]. BOLD activations from each of four cerebral hemispheres were projected onto the subjects' cortical surfaces and aligned to a surface-based atlas for comparison across hemispheres and subjects. This surface-based analysis revealed patterns of visuo-oculomotor activity across much of the cerebral cortex, including activations in the posterior parietal cortex, superior temporal cortex and frontal lobe. For each cortical domain, we show the anatomical position and extent of visuo-oculomotor activity, including evidence that the dorsolateral frontal activation, which includes the frontal eye field (on the anterior bank of the arcuate sulcus), extends anteriorly into posterior principal sulcus (area 46) and posteriorly into part of dorsal premotor cortex (area 6). Our results also suggest that subcortical BOLD activity in the pulvinar thalamus may be lateralized during voluntary eye movements. These findings provide new neuroanatomical information as to the complex neural substrates that underlie even simple goal-directed behaviors.
Non-spatial, motor-specific activation in posterior parietal cortex.
J. L. Calton, A. R. Dickinson, and L. H. Snyder
A localized cluster of neurons in macaque posterior parietal cortex, termed the parietal reach region (PRR), is activated when a reach is planned to a visible or remembered target. To explore the role of PRR in sensorimotor transformations, we tested whether cells would be activated when a reach is planned to an as-yet unspecified goal. Over one-third of PRR cells increased their firing after an instruction to prepare a reach, but not after an instruction to prepare a saccade, when the target of the movement remained unknown. A partially overlapping population (two-thirds of cells) was activated when the monkey was informed of the target location but not the type of movement to be made. Thus a subset of PRR neurons separately code spatial and effector-specific information, consistent with a role in specifying potential motor responses to particular targets.
Single neurons in posterior parietal cortex of monkeys encode cognitive set.
G. Stoet and L. H. Snyder
The primate posterior parietal cortex (PPC), part of the dorsal visual pathway, is best known for its role in encoding salient spatial information. Yet there are indications that neural activity in the PPC can also be modulated by nonspatial task-related information. In this study, we tested whether neurons in the PPC encode signals related to cognitive set, that is, the preparation to perform a particular task. Cognitive set has previously been associated with the frontal cortex but not the PPC. In this study, monkeys performed a cognitive set shifting paradigm in which they were cued in advance to apply one of two different task rules to the subsequent stimulus on every trial. Here we show that a subset of neurons in the PPC, concentrated in the lateral bank of the intraparietal sulcus and on the angular gyrus, responds selectively to cues for different task rules.
Nonspatial saccade-specific activation in area LIP of monkey parietal cortex.
A. R. Dickinson, J. L. Calton, and L. H. Snyder
We present evidence that neurons in the lateral intraparietal area (LIP) of monkey posterior parietal cortex (PPC) are activated by the instruction to make an eye movement, even in the complete absence of a spatial target. This study employed a visually guided motor task that dissociated the type of movement to make (saccade or reach) from the location where the movement was to be made. Using this task, animals were instructed to prepare a specific type of movement prior to knowing the spatial location of the movement target. We found that 25% of the LIP neurons recorded in two animals were activated significantly more by the instruction to prepare a saccade than by the instruction to prepare a reach. This finding indicates that LIP is involved in more than merely spatial attention and provides further evidence for nonspatial effector-specific signal processing in the dorsal stream.
Activity of neurons in the lateral intraparietal area of the monkey during an antisaccade task.
J. Gottlieb and M. E. Goldberg
The close relationship between saccadic eye movements and vision complicates the identification of neural responses associated with each function. Visual and saccade-related responses are especially closely intertwined in a subdivision of posterior parietal cortex, the lateral parietal area (LIP). We analyzed LIP neurons using an antisaccade task in which monkeys made saccades away from a salient visual cue. The vast majority of neurons reliably signaled the location of the visual cue. In contrast, most neurons had only weak, if any, saccade-related activity independent of visual stimulation. Thus, whereas the great majority of LIP neurons reliably encoded cue location, only a small minority encoded the direction of the upcoming saccade.
The lateral intraparietal area as a salience map: the representation of abrupt onset, stimulus motion, and task relevance.
M. Kusunoki, J. Gottlieb, and M. E. Goldberg
Neurons in the lateral intraparietal area (LIP) of the monkey represent salient stimuli. They respond to recently flashed stimuli that enter their receptive fields by virtue of saccades better than they respond to stable, behaviorally irrelevant stimuli brought into their receptive fields by saccades. They respond transiently to abrupt motion onsets, but have no directional selectivity. They respond to stable stimuli that are the targets for saccadic eye movements, but far less before the same saccades without stimuli. LIP is important in the attentional mechanisms preceding the choice of saccade target rather than in the intention to generate the saccade itself.
Response of neurons in the lateral intraparietal area to a distractor flashed during the delay period of a memory-guided saccade.
K. D. Powell and M. E. Goldberg
Recent experiments raised the possibility that the lateral intraparietal area (LIP) might be specialized for saccade planning. If this was true, one would expect a decreased sensitivity to irrelevant visual stimuli appearing late in the delay period of a memory-guided delayed-saccade task to a target outside the neurons' receptive fields. We trained two monkeys to perform a standard memory-guided delayed-saccade task and a distractor task in which a stimulus flashed for 200 ms at a predictable time 300-100 ms before the end of the delay period. We used two locations, one in the most active part of the receptive field and another well outside the receptive field. We used six kinds of trials randomly intermixed: simple delayed-saccade trials into or away from the receptive field and distractor trials with saccade target and distractor both in the receptive field, both out of the receptive field, or one at each location. This enabled us to study the response to the distractor as a function of the monkey's preparation of a memory-guided delayed-saccade task. We had assumed that the preparation of a saccade away from the receptive field would result in an attenuation of the response to the distractor, i.e., a distractor at the location of the saccade goal would evoke a greater response than when it appeared at a location far from the saccade goal. Instead we found that neurons exhibited either a normal or an enhanced visual response to the distractor during the memory period when the target flashed outside the receptive field. When the distractor flashed at the location of the saccade target, the response to the distractor was either unchanged or diminished. The response to a distractor away from the target location of a memory-guided saccade was even greater than the response to the same target when it was the target for the memory-guided saccade task. Immediate presaccadic activity did not distinguish between a saccade to the receptive field when there was no distractor and a distractor in the receptive field when the monkey made a saccade elsewhere. Nonetheless the distractor had no significant effect on the saccade latency, accuracy, or velocity despite the brisk response it evoked immediately before the saccade. We suggest that these results are inconsistent with a role for LIP in the specific generation of saccades, but they are consistent with a role for LIP in the generation of visual attention.
Dependence of saccade-related activity in the primate superior colliculus on visual target presence.
J. A. Edelman and M. E. Goldberg
Neurons in the intermediate layers of the superior colliculus respond to visual targets and/or discharge immediately before and during saccades. These visual and motor responses have generally been considered independent, with the visual response dependent on the nature of the stimulus, and the saccade-related activity related to the attributes of the saccade, but not to how the saccade was elicited. In these experiments we asked whether saccade-related discharge in the superior colliculus depended on whether the saccade was directed to a visual target. We recorded extracellular activity of neurons in the intermediate layers of the superior colliculus of three rhesus monkeys during saccades in tasks in which we varied the presence or absence of a visual target and the temporal delays between the appearance and disappearance of a target and saccade initiation. Across our sample of neurons (n = 64), discharge was highest when a saccade was made to a still-present visual target, regardless of whether the target had recently appeared or had been present for several hundred milliseconds. Discharge was intermediate when the target had recently disappeared and lowest when the target had never appeared during that trial. These results are consistent with the hypothesis that saccade-related discharge decreases as the time between the target disappearance and saccade initiation increases. Saccade velocity was also higher for saccades to visual targets, and correlated on a trial-by-trial basis with perisaccadic discharge for many neurons. However, discharge of many neurons was dependent on task but independent of saccade velocity, and across our sample of neurons, saccade velocity was higher for saccades made immediately after target appearance than would be predicted by discharge level. A tighter relationship was found between saccade precision and perisaccadic discharge. These findings suggest that just as the purpose of the saccadic system in primates is to drive the fovea to a visual target, presaccadic motor activity in the superior colliculus is most intense when such a target is actually present. This enhanced activity may, itself, contribute to the enhanced performance of the saccade system when the saccade is made to a real visual target.
Neural correlates of attention and distractibility in the lateral intraparietal area.
J. W. Bisley and M. E. Goldberg
We examined the activity of neurons in the lateral intraparietal area (LIP) during a task in which we measured attention in the monkey, using an advantage in contrast sensitivity as our definition of attention. The animals planned a memory-guided saccade but made or canceled it depending on the orientation of a briefly flashed probe stimulus. We measured the monkeys' contrast sensitivity by varying the contrast of the probe. Both subjects had better thresholds at the goal of the saccade than elsewhere. If a task-irrelevant distractor flashed elsewhere in the visual field, the attentional advantage transiently shifted to that site. The population response in LIP correlated with the allocation of attention; the attentional advantage lay at the location in the visual field whose representation in LIP had the greatest activity when the probe appeared. During a brief period in which there were two equally active regions in LIP, there was no attentional advantage at either location. This time, the crossing point, differed in the two animals, proving a strong correlation between the activity and behavior. The crossing point of each neuron depended on the relationship of three parameters: the visual response to the distractor, the saccade-related delay activity, and the rate of decay of the transient response to the distractor. Thus the time at which attention lingers on a distractor is set by the mechanism underlying these three biophysical properties. Finally, we showed that for a brief time LIP neurons showed a stronger response to signal canceling the planned saccade than to the confirmation signal.
Activity in the lateral intraparietal area predicts the goal and latency of saccades in a free-viewing visual search task.
A. E. Ipata, A. L. Gee, M. E. Goldberg, and J. W. Bisley
The purpose of saccadic eye movements is to facilitate vision, by placing the fovea on interesting objects in the environment. Eye movements are not made for reward, and they are rarely restricted. Despite this, most of our knowledge about the neural genesis of eye movements comes from experiments in which specific eye movements are rewarded or restricted. Such experiments have demonstrated that activity in the lateral intraparietal (LIP) area of the monkey correlates with the monkey's planning of a memory-guided saccade or deciding where, on the basis of motion information, to make a saccade. However, other experiments have shown that neural activity in LIP can easily be dissociated from the generation of saccadic eye movements, especially when sophisticated behavioral paradigms dissociate the monkey's locus of attention from the goal of an intended saccade. In this study, we trained monkeys to report the results of a visual search task by making a nontargeting hand movement. Once the task began, the monkeys were entirely free to move their eyes, and rewards were not contingent on the monkeys making specific eye movements. We found that neural activity in LIP predicted not only the goal of the monkey's saccades but also their saccadic latencies.
LIP responses to a popout stimulus are reduced if it is overtly ignored.
A. E. Ipata, A. L. Gee, J. Gottlieb, J. W. Bisley, and M. E. Goldberg
Bright objects capture our attention by virtue of 'popping out' from their surroundings. This correlates with strong responses in cortical areas thought to be important in attentional allocation. Previous studies have suggested that with the right mindset or training, humans can ignore popout stimuli. We studied the activity of neurons in monkey lateral intraparietal area while monkeys performed a visual search task. The monkeys were free to move their eyes, and a distractor, but never the search target, popped out. On trials in which the monkeys made a saccade directly to the search target, the popout distractor evoked a smaller response than the non-popout distractors. The intensity of the response to the popout correlated inversely with the monkeys' ability to ignore it. We suggest that this modulation corresponds to a top-down mechanism that the brain uses to adjust the parietal representation of salience.
Motor intention activity in the macaque's lateral intraparietal area. I. Dissociation of motor plan from sensory memory.
P. Mazzoni, R. M. Bracewell, S. Barash, and R. A. Andersen
1. The lateral intraparietal area (area LIP) of the monkey's posterior parietal cortex (PPC) contains neurons that are active during saccadic eye movements. These neurons' activity includes visual and saccade-related components. These responses are spatially tuned and the location of a neuron's visual receptive field (RF) relative to the fovea generally overlaps its preferred saccade amplitude and direction (i.e., its motor field, MF). When a delay is imposed between the presentation of a visual stimulus and a saccade made to its location (memory saccade task), many LIP neurons maintain elevated activity during the delay (memory activity, M), which appears to encode the metrics of the next intended saccadic eye movements. Recent studies have alternatively suggested that LIP neurons encode the locations of visual stimuli regardless of where the animal intends to look. We examined whether the M activity of LIP neurons specifically encodes movement intention or the locations of recent visual stimuli, or a combination of both. In the accompanying study, we investigated whether the intended-movement activity reflects changes in motor plan. 2. We trained monkeys (Macaca mulatta) to memorize the locations of two visual stimuli and plan a sequence of two saccades, one to each remembered target, as we recorded the activity of single LIP neurons. Two targets were flashed briefly while the monkey maintained fixation; after a delay the fixation point was extinguished, and the monkey made two saccades in sequence to each target's remembered location, in the order in which the targets were presented. This "delayed double saccade" (DDS) paradigm allowed us to dissociate the location of visual stimulation from the direction of the planned saccade and thus distinguish neuronal activity related to the target's location from activity related to the saccade plan. By imposing a delay, we eliminated the confounding effect of any phasic responses coincident with the appearance of the stimulus and with the saccade. 3. We arranged the two visual stimuli so that in one set of conditions at least the first one was in the neuron's visual RF, and thus the first saccade was in the neuron's motor field (MF). M activity should be high in these conditions according to both the sensory memory and motor plan hypotheses. In another set of conditions, the second stimulus appeared in the RF but the first one was presented outside the RF, instructing the monkey to plan the first saccade away from the neuron's MF. If the M activity encodes the motor plan, it should be low in these conditions, reflecting the plan for the first saccade (away from the MF). If it is a sensory trace of the stimulus' location, it should be high, reflecting stimulation of the RF by the second target. 4. We tested 49 LIP neurons (in 3 hemispheres of 2 monkeys) with M activity on the DDS task. Of these, 38 (77%) had M activity related to the next intended saccade. They were active in the delay period, as expected, if the first saccade was in their preferred direction. They were less active or silent if the next saccade was not in their preferred direction, even when the second stimulus appeared in their RF. 5. The M activity of 8 (16%) of the remaining neurons specifically encoded the location of the most recent visual stimulus. Their firing rate during the delay reflected stimulation of the RF independently of the saccade being planned. The remaining 3 neurons had M activity that did not consistently encode either the next saccade or the stimulus' location. 6. We also recorded the activity of a subset of neurons (n = 38) in a condition in which no stimulus appeared in a neuron's RF, but the second saccade was in the neuron's MF. In this case the majority of neurons tested (23/38, 60%) became active in the period between the first and second saccade, even if neither stimulus had appeared in their RF. Moreover, this activity appeared only after the first saccade had started in all but two of
Motor intention activity in the macaque's lateral intraparietal area. II. Changes of motor plan.
R. M. Bracewell, P. Mazzoni, S. Barash, and R. A. Andersen
1. In the companion paper we reported that the predominant signal of the population of neurons in the lateral intraparietal area (area LIP) of the monkey's posterior parietal cortex (PPC) encode the next intended saccadic eye movement during the delay period of a memory-saccade task. This result predicts that, should be monkey change his intention of what the next saccade will be, LIP activity should change accordingly to reflect the new plan. We tested this prediction by training monkeys to change their saccadic plan on command and recording the activity of LIP neurons across plan changes. 2. We trained rhesus monkeys (Macaca mulatta) to maintain fixation on a light spot as long as this spot remained on. During this period we briefly presented one, two, or three peripheral visual stimuli in sequence, each followed by a delay (memory period, M). After the final delay the fixation spot was extinguished, and the monkey had to quickly make a saccade to the location of the last target to have appeared. The monkey could not predict which stimuli, nor how many, would appear on each trial. He thus had to plan a saccade to each stimulus as it appeared and change his saccade plan whenever a stimulus appeared at a different location. 3. We recorded the M period activity of 81 area LIP neurons (from 3 hemispheres of 2 monkeys) in this task. We predicted that, if a neuron's activity reflected the monkey's planned saccade, its activity should be high while the monkey planned a saccade in the neuron's motor field (MF), and low while the planned saccade was in the opposite direction. The activity of most of the neurons in our sample changed in accordance with our hypothesis as the monkey's planned saccade changed. 4. In one condition the monkey was instructed by visual stimuli to change his plan from a saccade in the neuron's preferred direction to a saccade planned in the opposite direction. In this condition activity decreased significantly (P < 0.05) in 65 (80%) of 81 neurons tested. These neurons' activity changed to reflect the new saccade plan even though the cue for this change was not presented in their RF. 5. As a control we randomly interleaved, among trials requiring a plan change, trials in which the monkey had to formulate two consecutive plans to make a saccade in the neuron's preferred direction. The activity remained unchanged (P < 0.05) in 22 of 31 neurons tested (79%), indicating that the neurons continued to encode the same saccade plan. 6. In a variant of the task, the cue to the location of the required saccade was either a light spot or a noise burst from a loudspeaker. Of 22 neurons tested in this task, 16 (73%) showed activity changes consistent with plan changes cued by visual or auditory stimuli. 7. Alterations in the monkey's intentions, even in the absence of overt behavior, are manifested in altered LIP activity. These activity changes could be induced whether visual or auditory cues were used to indicate the required plan changes. Most LIP neurons thus do not encode only the locations of visual stimuli, but also the intention to direct gaze to specific locations, independently of whether a gaze shift actually occurs.
Coding of intention in the posterior parietal cortex.
L. H. Snyder, A. P. Batista, and R. A. Andersen
To look at or reach for what we see, spatial information from the visual system must be transformed into a motor plan. The posterior parietal cortex (PPC) is well placed to perform this function, because it lies between visual areas, which encode spatial information, and motor cortical areas. The PPC contains several subdivisions, which are generally conceived as high-order sensory areas. Neurons in area 7a and the lateral intraparietal area fire before and during visually guided saccades. Other neurons in areas 7a and 5 are active before and during visually guided arm movements. These areas are also active during memory tasks in which the animal remembers the location of a target for hundreds of milliseconds before making an eye or arm movement. Such activity could reflect either visual attention or the intention to make movements. This question is difficult to resolve, because even if the animal maintains fixation while directing attention to a peripheral location, the observed neuronal activity could reflect movements that are planned but not executed. To address this, we recorded from the PPC while monkeys planned either reaches or saccades to a single remembered location. We now report that, for most neurons, activity before the movement depended on the type of movement being planned. We conclude that PPC contains signals related to what the animal intends to do.
Parietal representation of object-based saccades.
P. N. Sabes, B. Breznen, and R. A. Andersen
When monkeys make saccadic eye movements to simple visual targets, neurons in the lateral intraparietal area (LIP) display a retinotopic, or eye-centered, coding of the target location. However natural saccadic eye movements are often directed at objects or parts of objects in the visual scene. In this paper we investigate whether LIP represents saccadic eye movements differently when the target is specified as part of a visually displayed object. Monkeys were trained to perform an object-based saccade task that required them to make saccades to previously cued parts of an abstract object after the object reappeared in a new orientation. We recorded single neurons in area LIP of two macaque monkeys and analyzed their activity in the object-based saccade task, as well as two control tasks: a standard memory saccade task and a fixation task with passive object viewing. The majority of LIP neurons that were tuned in the memory saccade task were also tuned in the object-based saccade task. Using a hierarchical generalized linear model analysis, we compared the effects of three different spatial variables on the firing rate: the retinotopic location of the target, the object-fixed location of the target, and the orientation of the object in space. There was no evidence of an explicit object-fixed representation in the activity in LIP during either of the object-based tasks. In other words, no cells had receptive fields that rotated with the object. While some cells showed a modulation of activity due to the location of the target on the object, these variations were small compared to the retinotopic effects. For most cells, firing rates were best accounted for by either the retinotopic direction of the movement, the orientation of the object, or both spatial variables. The preferred direction of these retinotopic and object orientation effects were found to be invariant across tasks. On average, the object orientation effects were consistent with the retinotopic coding of potential target locations on the object. This interpretation is supported by the fact that the magnitude of these two effects were roughly equal in the early portions of the trial, but around the time of the motor response, the retinotopic effects dominated. We conclude that LIP uses the same retinotopic coding of saccade target whether the target is specified as an absolute point in space or as a location on a moving object.