Spike-field activity in parietal area LIP during coordinated reach and saccade movements

The posterior parietal cortex is situated between visual and motor areas and supports coordinated visually guided behavior. Area LIP in the intraparietal sulcus contains representations of visual space and has been extensively studied in the context of saccades. However, area LIP has not been studied during coordinated movements, so it is not known whether saccadic representations in area LIP are influenced by coordinated behavior. Here, we studied spiking and local field potential (LFP) activity in area LIP while subjects performed coordinated reaches and saccades or saccades alone to remembered target locations to test whether activity in area LIP is influenced by the presence of a coordinated reach. We find that coordination significantly changes the activity of individual neurons in area LIP, increasing or decreasing the firing rate when a reach is made with a saccade compared with when a saccade is made alone. Analyzing spike-field coherence demonstrates that area LIP neurons whose firing rate is suppressed during the coordinated task have activity temporally correlated with nearby LFP activity, which reflects the synaptic activity of populations of neurons. Area LIP neurons whose firing rate increases during the coordinated task do not show significant spike-field coherence. Furthermore, LFP power in area LIP is suppressed and does not increase when a coordinated reach is made with a saccade. These results demonstrate that area LIP neurons display different responses to coordinated reach and saccade movements, and that different spike rate responses are associated with different patterns of correlated activity. The population of neurons whose firing rate is suppressed is coherently active with local populations of LIP neurons. Overall, these results suggest that area LIP plays a role in coordinating visually guided actions through suppression of coherent patterns of saccade-related activity.     

Nonspatial saccade-specific activation in area LIP of monkey parietal cortex

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.     

Spatial updating in area LIP is independent of saccade direction

We explore the world around us by making rapid eye movements to objects of interest. Remarkably, these eye movements go unnoticed, and we perceive the world as stable. Spatial updating is one of the neural mechanisms that contributes to this perception of spatial constancy. Previous studies in macaque lateral intraparietal cortex (area LIP) have shown that individual neurons update, or "remap," the locations of salient visual stimuli at the time of an eye movement. The existence of remapping implies that neurons have access to visual information from regions far beyond the classically defined receptive field. We hypothesized that neurons have access to information located anywhere in the visual field. We tested this by recording the activity of LIP neurons while systematically varying the direction in which a stimulus location must be updated. Our primary finding is that individual neurons remap stimulus traces in multiple directions, indicating that LIP neurons have access to information throughout the visual field. At the population level, stimulus traces are updated in conjunction with all saccade directions, even when we consider direction as a function of receptive field location. These results show that spatial updating in LIP is effectively independent of saccade direction. Our findings support the hypothesis that the activity of LIP neurons contributes to the maintenance of spatial constancy throughout the visual field.     

TMS modulation of visual and auditory processing in the posterior parietal cortex

The activity patterns of a neuronal network originate from the intrinsic properties and synaptic interactions of the constituent neurons. Our recent studies support this view, showing that the discharge of a single frog retina ganglion cell brings an elementary neuronal network of the tectum (tectum column) to a suprathreshold activity of two distinct levels that are related to the activation of the slow L-type calcium current in dendrites of the recurrent pear-shaped neurons (lower level) and the NMDA receptors in neurons (higher level) of the tectum column. We show in the present study that the dendritic slow L-type calcium current is necessary for the NMDA receptor activation in the tectum column. A small decrease of this current prevents the NMDA receptor activation and, hence, the transition of the network to the higher activity level, at which the efferent neuron of the network fires. So, the activity of the frog tectum column can be effectively controlled through the intrinsic properties of the recurrent pear-shaped neurons of the column.     

Superior colliculus activity related to concurrent processing of saccade goals in a visual search task

Saccades are typically separated by inter-saccadic fixation intervals (ISFIs) of > or =125 ms. During this time, the saccadic system selects a goal and completes the preparatory processes required prior to executing the subsequent movement. However, in tasks in which competing stimuli are presented, two sequentially executed movements to different goals can be separated by much shorter ISFIs. This suggests that the saccadic system is capable of completing many of the preparatory requirements for a second saccade concurrently with the execution of an initial movement. We recorded single neurons in the superior colliculus (SC) during rapid saccade sequences made by rhesus monkeys performing a search task. We found that during the execution of an initial saccade, activity related to the goal of a quickly following second saccade can be simultaneously maintained in the SC motor map. This activity appears to signal the selection or increased salience of the second saccade goal even before the initial saccade has ended. For movements separated by normal ISFIs (> or =125 ms), we did not observe activity related to concurrent processing, presumably because for these longer ISFI responses, the goal of the second saccade is not selected until after the end of the first saccade. These results indicate that, at the time of an initial saccade, the SC does not necessarily act as a strict winner-take-all network. Rather it appears that the salience of a second visual goal can be simultaneously maintained in the SC. This provides evidence that selection or preparatory activity related to the goal of a second saccade can overlap temporally with activity related to an initial saccade and indicates that such concurrent processing is present even in a structure which is fairly close to the motor output.     

Dissociation of visual, motor and predictive signals in parietal cortex during visual guidance

The role of the posterior parietal cortex (PPC) in the visual guidance of movements was studied in monkeys trained to use a joystick to guide a spot to a target. Visual and motor influences were dissociated by transiently occluding the spot and by varying the relationship between the direction of joystick and spot movements. We found a strong segregation of function in PPC during visual guidance. Neurons in area MST were selectively modulated by the direction of visible moving stimuli, whereas neurons in area MIP were selectively modulated by the direction of hand movement. In contrast, the selectivity of cells in the lateral intraparietal area (LIP) did not directly depend on either visual input or motor output, but rather seemed to encode a predictive representation of stimulus movement. These predictive signals may be an important link in visuomotor transformations.     

Neural basis of a perceptual decision in the parietal cortex (area LIP) of the rhesus monkey

We recorded the activity of single neurons in the posterior parietal cortex (area LIP) of two rhesus monkeys while they discriminated the direction of motion in random-dot visual stimuli. The visual task was similar to a motion discrimination task that has been used in previous investigations of motion-sensitive regions of the extrastriate cortex. The monkeys were trained to decide whether the direction of motion was toward one of two choice targets that appeared on either side of the random-dot stimulus. At the end of the trial, the monkeys reported their direction judgment by making an eye movement to the appropriate target. We studied neurons in LIP that exhibited spatially selective persistent activity during delayed saccadic eye movement tasks. These neurons are thought to carry high-level signals appropriate for identifying salient visual targets and for guiding saccadic eye movements. We arranged the motion discrimination task so that one of the choice targets was in the LIP neuron's response field (RF) while the other target was positioned well away from the RF. During motion viewing, neurons in LIP altered their firing rate in a manner that predicted the saccadic eye movement that the monkey would make at the end of the trial. The activity thus predicted the monkey's judgment of motion direction. This predictive activity began early in the motion-viewing period and became increasingly reliable as the monkey viewed the random-dot motion. The neural activity predicted the monkey's direction judgment on both easy and difficult trials (strong and weak motion), whether or not the judgment was correct. In addition, the timing and magnitude of the response was affected by the strength of the motion signal in the stimulus. When the direction of motion was toward the RF, stronger motion led to larger neural responses earlier in the motion-viewing period. When motion was away from the RF, stronger motion led to greater suppression of ongoing activity. Thus the activity of single neurons in area LIP reflects both the direction of an impending gaze shift and the quality of the sensory information that instructs such a response. The time course of the neural response suggests that LIP accumulates sensory signals relevant to the selection of a target for an eye movement.     

Temporal structure in neuronal activity during working memory in macaque parietal cortex

Many cortical structures have elevated firing rates during working memory, but it is not known how the activity is maintained. To investigate whether reverberating activity is important, we studied the temporal structure of local field potential (LFP) activity and spiking from area LIP in two awake macaques during a memory-saccade task. Using spectral analysis, we found spatially tuned elevated power in the gamma band (25-90 Hz) in LFP and spiking activity during the memory period. Spiking and LFP activity were also coherent in the gamma band but not at lower frequencies. Finally, we decoded LFP activity on a single-trial basis and found that LFP activity in parietal cortex discriminated between preferred and anti-preferred direction with approximately the same accuracy as the spike rate and predicted the time of a planned movement with better accuracy than the spike rate. This finding could accelerate the development of a cortical neural prosthesis.     

Role for human posterior parietal cortex in visual processing of aversive objects in peripersonal space

The posterior parietal cortex of both human and non-human primates is known to play a crucial role in the early integration of visual information with somatosensory, proprioceptive and vestibular signals. However, it is not known whether in humans this region is further capable of discriminating if a stimulus poses a threat to the body. In this functional magnetic resonance imaging (fMRI) study, we tested the hypothesis that the posterior parietal cortex of humans is capable of modulating its response to the visual processing of noxious threat representation in the absence of tactile input. During fMRI, participants watched while we "stimulated" a visible rubber hand, placed over their real hand with either a sharp (painful) or a blunt (nonpainful) probe. We found that superior and inferior parietal regions (BA5/7 and BA40) increased their activity in response to observing a painful versus nonpainful stimulus. However, this effect was only evident when the rubber hand was in a spatially congruent (vs. incongruent) position with respect to the participants' own hand. In addition, areas involved in motivational-affective coding such as mid-cingulate (BA24) and anterior insula also showed such relevance-dependent modulation, whereas premotor areas known to receive multisensory information about limb position did not. We suggest these results reveal a human anatomical-functional homologue to monkey inferior parietal areas that respond to aversive stimuli by producing nocifensive muscle and limb movements.     

Dissociating the contributions of human frontal eye fields and posterior parietal cortex to visual search

Imaging, lesion, and transcranial magnetic stimulation (TMS) studies have implicated a number of regions of the brain in searching for a target defined by a combination of attributes. The necessity of both frontal eye fields (FEF) and posterior parietal cortex (PPC) in task performance has been shown by the application of TMS over these regions. The effects of stimulation over these two areas have, thus far, proved to be remarkably similar and the only dissociation reported being in the timing of their involvement. We tested the hypotheses that 1) FEF contributes to performance in terms of visual target detection (possibly by modulation of activity in extrastriate areas with respect to the target), and 2) PPC is involved in translation of visual information for action. We used a task where the presence (and location) of the target was indicated by an eye movement. Task disruption was seen with FEF TMS (with reduced accuracy on the task) but not with PPC stimulation. When a search task requiring a manual response was presented, disruption with PPC TMS was seen. These results show dissociation of FEF and PPC contributions to visual search performance and that PPC involvement seems to be dependent on the response required by the task, whereas this is not the case for FEF. This supports the idea of FEF involvement in visual processes in a manner that might not depend on the required response, whereas PPC seems to be involved when a manual motor response to a stimulus is required.     

The retinotopic match between area 17 and its targets in visual suprasylvian cortex

Summary It is widely believed that cells in area 17 send axons specifically to neurons in other cortical areas whose receptive fields coincide with their own. We asked whether this was true in cats for area 17's projection to a large suprasylvian visual area, the Clare-Bishop area. Receptive fields were plotted at multiple sites in the Clare-Bishop area. Then, in area 17, anterograde tracer was injected at a retinotopically-characterized site, giving rise to patches of labeled terminals in the Clare-Bishop area. Receptive field centers recorded within these patches were located close to the visual field location at the injection site in area 17. Receptive fields recorded outside of labeled patches, on the other hand, were never in register with that plotted in area 17. However, due to their large size, even fields located outside of labeled patches often encompassed the visual field point injected in area 17. In other experiments, receptive fields for both neurons and presumed cortical afferents were recorded at the same site in the Clare-Bishop area. The centers of such pairs of receptive fields were on average less than 1° apart. Finally, the gaps between widely separated patches of label were investigated. Both physiological and anatomical evidence indicated that a different part of the visual field was represented in gaps than in the adjacent patches.     

Involvement of prefrontal cortex in visual search

Visual search for target items embedded within a set of distracting items has consistently been shown to engage regions of occipital and parietal cortex, but the contribution of different regions of prefrontal cortex remains unclear. Here, we used fMRI to compare brain activity in 12 healthy participants performing efficient and inefficient search tasks in which target discriminability and the number of distractor items were manipulated. Matched baseline conditions were incorporated to control for visual and motor components of the tasks, allowing cortical activity associated with each type of search to be isolated. Region of interest analysis was applied to critical regions of prefrontal cortex to determine whether their involvement was common to both efficient and inefficient search, or unique to inefficient search alone. We found regions of the inferior and middle frontal cortex were only active during inefficient search, whereas an area in the superior frontal cortex (in the region of FEF) was active for both efficient and inefficient search. Thus, regions of ventral as well as dorsal prefrontal cortex are recruited during inefficient search, and we propose that this activity is related to processes that guide, control and monitor the allocation of selective attention.     

Preferential encoding of visual categories in parietal cortex compared with prefrontal cortex

The ability to recognize the behavioral relevance, or category membership, of sensory stimuli is critical for interpreting the meaning of events in our environment. Neurophysiological studies of visual categorization have found categorical representations of stimuli in prefrontal cortex (PFC), an area that is closely associated with cognitive and executive functions. Recent studies have also identified neuronal category signals in parietal areas that are typically associated with visual-spatial processing. It has been proposed that category-related signals in parietal cortex and other visual areas may result from 'top-down' feedback from PFC. We directly compared neuronal activity in the lateral intraparietal (LIP) area and PFC in monkeys performing a visual motion categorization task. We found that LIP showed stronger, more reliable and shorter latency category signals than PFC. These findings suggest that LIP is strongly involved in visual categorization and argue against the idea that parietal category signals arise as a result of feedback from PFC during this task.     

Integration of motor and visual information in the parietal area 5 during locomotion

The parietal cortex receives both visual- and motor-related information and is believed to be one of the sites of visuo-motor coordination. This study for the first time characterizes integration of visual and motor information in activity of neurons of parietal area 5 during locomotion under conditions that require visuo-motor coordination. The activity of neurons was recorded in cats during walking on a flat surface-a task with no visuo-motor coordination required (flat locomotion), walking along a horizontal ladder or a series of barriers-a task requiring visuo-motor coordination for an accurate foot placement on surface that is heterogeneous along the direction of progression (ladder and barriers locomotion), and walking along a narrow pathway-a task requiring visuo-motor coordination on surface homogeneous along the direction of progression (narrow locomotion). During flat locomotion, activity of 66% of the neurons was modulated in rhythm of stepping, usually with one peak per cycle. During ladder and barrier locomotion, the proportion of rhythmically active neurons significantly increased, their modulation became stronger, and the majority of neurons had two peaks of activity per cycle. During narrow locomotion, however, the activity of neurons was similar to that during flat locomotion. We concluded that, during locomotion, parietal area 5 integrates two types of information: signals about the activity of basic locomotion mechanisms and signals about heterogeneity of the surface along the direction of progression. We describe here the modes of integration of these two types of information during locomotion.     

Feature processing during visual search in normal aging: electrophysiological evidence

Event-related potentials (ERPs) were recorded from healthy young and older subjects during the execution of a visual search task in which they were required to detect the presence of a target stimulus that differed from distractors in a salient feature (orientation). Apart from the orientation target, a task-irrelevant singleton defined by a different feature (color) was also presented without instruction. The effects of normal aging on the N2pc component, an electrophysiological correlate of the allocation of visuospatial attention, were evaluated for the first time. Behavioral results showed an increase in the mean reaction time (RT) and a reduction in the hit rates with age. Electrophysiological results showed a consistent N2pc for orientation target pop-outs but not for irrelevant color pop-outs in both age groups, suggesting that the irrelevant color singleton did not induce attentional capture. Furthermore, the N2pc component observed for orientation targets was significantly delayed and attenuated in older subjects compared to young subjects, suggesting a specific impairment of the allocation of visuospatial attention with advancing age.     

Topographic maps of visual spatial attention in human parietal cortex

Functional magnetic resonance imaging (fMRI) was used to measure activity in human parietal cortex during performance of a visual detection task in which the focus of attention systematically traversed the visual field. Critically, the stimuli were identical on all trials (except for slight contrast changes in a fully randomized selection of the target locations) whereas only the cued location varied. Traveling waves of activity were observed in posterior parietal cortex consistent with shifts in covert attention in the absence of eye movements. The temporal phase of the fMRI signal in each voxel indicated the corresponding visual field location. Visualization of the distribution of temporal phases on a flattened representation of parietal cortex revealed at least two distinct topographically organized cortical areas within the intraparietal sulcus (IPS), each representing the contralateral visual field. Two cortical areas were proposed based on this topographic organization, which we refer to as IPS1 and IPS2 to indicate their locations within the IPS. This nomenclature is neutral with respect to possible homologies with well-established cortical areas in the monkey brain. The two proposed cortical areas exhibited relatively little response to passive visual stimulation in comparison with early visual areas. These results provide evidence for multiple topographic maps in human parietal cortex.     

Memory-guided saccade processing in visual form agnosia (patient DF)

According to Milner and Goodale’s model (The visual brain in action, Oxford University Press, Oxford, 2006) areas in the ventral visual stream mediate visual perception and off-line actions, whilst regions in the dorsal visual stream mediate the on-line visual control of action. Strong evidence for this model comes from a patient (DF), who suffers from visual form agnosia after bilateral damage to the ventro-lateral occipital region, sparing V1. It has been reported that she is normal in immediate reaching and grasping, yet severely impaired when asked to perform delayed actions. Here we investigated whether this dissociation would extend to saccade execution. Neurophysiological studies and TMS work in humans have shown that the posterior parietal cortex (PPC), on the right in particular (supposedly spared in DF), is involved in the control of memory-guided saccades. Surprisingly though, we found that, just as reported for reaching and grasping, DF’s saccadic accuracy was much reduced in the memory compared to the stimulus-guided condition. These data support the idea of a tight coupling of eye and hand movements and further suggest that dorsal stream structures may not be sufficient to drive memory-guided saccadic performance.     

Brightness processing in the visual cortex

Single cell recordings have shown that some cells in the primary visual cortex (V1) signal surface brightness. However, fMRI experiments have found brightness related activation only in the higher cortical areas. In a psychophysical setup, we were able to dissociate the reduction of brightness caused by Gabor flankers, similar to the receptive fields in V1, from the edge induced brightness change. The former resemble the single cell recording results and the latter the fMRI results.     

Progression in neuronal processing for saccadic eye movements from parietal cortex area lip to superior colliculus

Neurons in both the lateral intraparietal area (LIP) of the monkey parietal cortex and the intermediate layers of the superior colliculus (SC) are activated well in advance of the initiation of saccadic eye movements. To determine whether there is a progression in the covert processing for saccades from area LIP to SC, we systematically compared the discharge properties of LIP output neurons identified by antidromic activation with those of SC neurons collected from the same monkeys. First, we compared activity patterns during a delayed saccade task and found that LIP and SC neurons showed an extensive overlap in their responses to visual stimuli and in their sustained activity during the delay period. The saccade activity of LIP neurons was, however, remarkably weaker than that of SC neurons and never occurred without any preceding delay activity. Second, we assessed the dependence of LIP and SC activity on the presence of a visual stimulus by contrasting their activity in delayed saccade trials in which the presentation of the visual stimulus was either sustained (visual trials) or brief (memory trials). Both the delay and the presaccadic activity levels of the LIP neuronal sample significantly depended on the sustained presence of the visual stimulus, whereas those of the SC neuronal sample did not. Third, we examined how the LIP and SC delay activity relates to the future production of a saccade using a delayed GO/NOGO saccade task, in which a change in color of the fixation stimulus instructed the monkey either to make a saccade to a peripheral visual stimulus or to withhold its response and maintain fixation. The average delay activity of both LIP and SC neuronal samples significantly increased by the advance instruction to make a saccade, but LIP neurons were significantly less dependent on the response instruction than SC neurons, and only a minority of LIP neurons was significantly modulated. Thus despite some overlap in their discharge properties, the neurons in the SC intermediate layers showed a greater independence from sustained visual stimulation and a tighter relationship to the production of an impending saccade than the LIP neurons supplying inputs to the SC. Rather than representing the transmission of one processing stage in parietal cortex area LIP to a subsequent processing stage in SC, the differences in neuronal activity that we observed suggest instead a progressive evolution in the neuronal processing for saccades.