Saccade-related activity in the lateral intraparietal area. II. Spatial properties.

1. Single-neuron activity was recorded from the inferior parietal lobule (IPL) of Macaca mulatta monkeys while they were performing delayed saccades and related tasks. Temporal characteristics of this activity were presented in the companion paper. Here we focus on the spatial characteristics of the activity. The analysis was based on recordings from 145 neurons. All these neurons were from the lateral intraparietal area (LIP), a recently defined subdivision of the IPL. 2. Delayed saccades were made in eight directions. Direction-tuning curves were calculated for each neuron, during each of the following activity phases that were described in the companion paper: light sensitive (LS), delay-period memory (M), and saccade related (S); the latter further partitioned into presaccadic (Pre-S), saccade coincident (S-Co), and postsaccadic (Post-S). 3. Width and preferred direction were calculated for each direction-tuning curve. We studied the distributions of widths and preferred directions in LIP's neuronal population. In each case we included only neurons that showed clear excitatory activity in the phases in question. 4. Width was defined as the angle over which the response was higher than 50% of its maximal net value. Width distributions were similar for all phases studied. Widths varied widely from neuron to neuron, from very narrow (less than 45 degrees) to very wide (close to 360 degrees). Median widths were approximately 90 degrees in all phases. 5. Preferred-direction distributions were also similar for various phases. All directions were represented in each distribution, but contralateral directions were more frequent (e.g., 69% for S-Co). 6. For each neuron the alignment of the preferred directions of its various phases was determined. Distributions of alignments were calculated (again, phases that were not clearly excitatory were disregarded). On the level of the neuronal population LS, M, and Pre-S were well aligned with each other. S-Co was also aligned with these phases, but less precisely. 7. A set of "narrowly tuned" neurons was selected by imposing a constraint of narrow (width, less than 90 degrees) LS and S-Co direction tuning. In this set of neurons, the LS and S-Co preferred directions were very well aligned (median, 12 degrees). The fraction of narrowly tuned neurons in the population was 40% (25/63). Thus, in a large subpopulation of area LIP, a fairly precise alignment exists between sensory and motor fields. 8. An additional set of 82 area LIP neurons were recorded while the monkey performed delayed saccades to 32 targets located on small, medium, and large imaginary circles.(ABSTRACT TRUNCATED AT 400 WORDS)     

Ocular fixation and visual activity in the monkey lateral intraparietal area

The macaque lateral intraparietal area (LIP) has been implicated in visuospatial attention and saccade planning. Since area LIP also contains a representation of the central visual field, we investigated its possible role in fixation and foveal attention in a visual fixation task with gap (momentary disappearance of fixation point). In addition to the expected visual neurons ( n=119), two main categories were identified: (1) cells responding tonically both during the presence and momentary absence of the fixation stimulus( n=47); a subset of these neurons studied in a saccade task showed perisaccadic inhibition in half of the cases (14/27). The timing of this inhibition, however, is only loosely related to saccade timing; (2) cells responding mainly to the absence of the fixation stimulus, with either abrupt or gradual onset of activity during the gap ( n=62). During saccades, these neurons showed presaccadic buildup and/or postsaccadic activity, which was spatially tuned in about half of the tested cells (28/53). Ninety-one percent of the cells in the first category and 59% of the cells in the second category were located in the dorsal portion of area LIP (LIPd). These results are consistent with the hypothesis of an oculomotor-attentional network contributing to fixation engagement and disengagement in a subregion of LIP.     

Responses to auditory stimuli in macaque lateral intraparietal area. I. Effects of training.

The lateral intraparietal area (LIP) of macaques has been considered unresponsive to auditory stimulation. Recent reports, however, indicate that neurons in this area respond to auditory stimuli in the context of an auditory-saccade task. Is this difference in auditory responsiveness of LIP due to auditory-saccade training? To address this issue, LIP responses in two monkeys were recorded at two different times: before and after auditory-saccade training. Before auditory-saccade training, the animals had never been trained on any auditory task, but had been trained on visual tasks. In both sets of experiments, activity of LIP neurons was recorded while auditory and visual stimuli were presented and the animals were fixating. Before training, 172 LIP neurons were recorded. Among these, the number of cells responding to auditory stimuli did not reach significance, whereas about one-half of the cells responded to visual stimuli. An information theory analysis confirmed that no information about auditory stimulus location was available in LIP neurons in the experiments before training. After training, activity from 160 cells was recorded. These experiments showed that 12% of cells in area LIP responded to auditory stimuli, whereas the proportion of cells responding to visual stimuli remained about the same as before training. The information theory analysis confirmed that, after training, information about auditory stimulus location was available in LIP neurons. Auditory-saccade training therefore generated responsiveness to auditory stimuli de novo in LIP neurons. Thus some LIP cells become active for auditory stimuli in a passive fixation task, once the animals have learned that these stimuli are important for oculomotor behavior.     

Direction selectivity of neurons in the macaque lateral intraparietal area

The lateral intraparietal area (LIP) of the macaque is believed to play a role in the allocation of attention and the plan to make saccadic eye movements. Many studies have shown that LIP neurons generally encode the static spatial location demarked by the receptive field (RF). LIP neurons might also provide information about the features of visual stimuli within the RF. For example, LIP receives input from cortical areas in the dorsal visual pathway that contain many direction-selective neurons. Here we examine direction selectivity of LIP neurons. Animals were only required to fixate while motion stimuli appeared in the RF. To avoid spatial confounds, the motion stimuli were patches of randomly arrayed dots that moved with 100% coherence in eight different directions. We found that the majority (61%) of LIP neurons were direction selective. The direction tuning was fairly broad, with a median direction-tuning bandwidth of 136 degrees. The average strength of direction selectivity was weaker in LIP than that of other areas of the dorsal visual stream but that difference may be because of the fact that LIP neurons showed a tonic offset in firing whenever a visual stimulus was in the RF, independent of direction. Direction-selective neurons do not seem to constitute a functionally distinct subdivision within LIP, because those neurons had robust, sustained delay-period activity during a memory delayed saccade task. The direction selectivity could also not be explained by asymmetries in the spatial RF, in the hypothetical case that the animals attended to slightly different locations depending on the direction of motion in the RF. Our results show that direction selectivity is a distinct attribute of LIP neurons in addition to spatial encoding.     

Spatial and non-spatial auditory processing in the lateral intraparietal area

We tested the responses of neurons in the lateral parietal area (area LIP) for their sensitivity to the spatial and non-spatial attributes of an auditory stimulus. We found that the firing rates of LIP neurons were modulated by both of these attributes. These data indicate that, while area LIP is involved in spatial processing, non-spatial processing is not restricted to independent channels.     

Neural correlates of attention and distractibility in the lateral intraparietal area

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.     

I. Functional properties of neurons in lateral part of associative area 7 in awake monkeys

Summary The lateral part of area 7, area 7b, of alert, behaving macaque monkeys was investigated using transdural microelectrode recording technique. Two hundred twenty-eight cells from five hemispheres of four monkeys were isolated and studied. The functional properties of 2% of the cells isolated remained unidentified. Functions of the identified cells were prominently related to the spatial control of arm movements.Of the cells 70% responded to somatosensory (40%) or visual (16%) or both somatosensory and visual (14%) stimulation. The receptive fields of these passively drivable cells were large, covering, e.g., the arm or leg or chest or even the skin of the whole body. Most of the visually drivable cells responded to stimuli in both halves of the visual field.Of the cells responding to sensory stimulation 80% were activated by stimuli moving in a certain direction. Of the directionally selective cells 25% received information through more than one sensory channel. The complex stimulus-response relationships of these convergence cells revealed the existence of an integrative system which analyzes the direction of a stimulus moving in one sensory system using an other sensory system as a reference.Of all the cells isolated 28% discharged only during active movements of the arms (25%) or eyes (3%). Firing of these neurons was related to contraction of a functionally uniform group of muscles and not individual muscles.Some previous investigations of the parietal association cortex, conducted mainly in area 7a, have shown that most cells are active only when the monkey himself moves his eyes or arms. In our study on area 7b most cells responded to passive stimulation. The discrepancy between the results indicates functional differentiation within area 7.     

Responses to auditory stimuli in macaque lateral intraparietal area. II. Behavioral modulation.

The lateral intraparietal area (LIP), a region of posterior parietal cortex, was once thought to be unresponsive to auditory stimulation. However, recent reports have indicated that neurons in area LIP respond to auditory stimuli during an auditory-saccade task. To what extent are auditory responses in area LIP dependent on the performance of an auditory-saccade task? To address this question, recordings were made from 160 LIP neurons in two monkeys while the animals performed auditory and visual memory-saccade and fixation tasks. Responses to auditory stimuli were significantly stronger during the memory-saccade task than during the fixation task, whereas responses to visual stimuli were not. Moreover, neurons responsive to auditory stimuli tended also to be visually responsive and to exhibit delay or saccade activity in the memory-saccade task. These results indicate that, in general, auditory responses in area LIP are modulated by behavioral context, are associated with visual responses, and are predictive of delay or saccade activity. Responses to auditory stimuli in area LIP may therefore be best interpreted as supramodal responses, and similar in nature to the delay activity, rather than as modality-specific sensory responses. The apparent link between auditory activity and oculomotor behavior suggests that the behavioral modulation of responses to auditory stimuli in area LIP reflects the selection of auditory stimuli as targets for eye movements.     

Responses of neurons in the lateral intraparietal area to central visual cues

Goal-directed behavior is characterized by flexible stimulus-action mappings. The lateral intraparietal area (area LIP) contains a representation of extra-personal space that is used to guide goal-directed behavior. To examine further how area LIP contributes to these flexible stimulus-action mappings, we recorded LIP activity while rhesus monkeys participated in two different cueing tasks. In the first task, the color of a central light indicated the location of a monkey’s saccadic endpoint in the absence of any other visual stimuli. In the second task, the color of a central light indicated which of two visual targets was the saccadic goal. In both tasks, LIP activity was modulated by these non-spatial cues. These observations further suggest a role for area LIP in mediating endogenous associations that link stimuli with actions.     

Activity of neurons in the lateral intraparietal area of the monkey during an antisaccade task.

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.     

Neurons in the lateral intraparietal area create a priority map by the combination of disparate signals

Primates search for objects in the visual field with eye movements. We recorded the activity of neurons in the lateral intraparietal area (LIP) in animals performing a visual search task in which they were free to move their eyes, and reported the results of the search with a hand movement. We distinguished three independent signals: (1) a visual signal describing the abrupt onset of a visual stimulus in the receptive field; (2) a saccadic signal predicting the monkey’s saccadic reaction time independently of the nature of the stimulus; (3) a cognitive signal distinguishing between the search target and a distractor independently of the direction of the impending saccade. The cognitive signal became significant on average 27 ms after the saccadic signal but before the saccade was made. The three signals summed in a manner discernable at the level of the single neuron. A.E. Ipata and A.L. Gee have contributed equally to this work.     

Frontal eye field microstimulation induces task-dependent gamma oscillations in the lateral intraparietal area

Macaque frontal eye fields (FEF) and the lateral intraparietal area (LIP) are high-level oculomotor control centers that have been implicated in the allocation of spatial attention. Electrical microstimulation of macaque FEF elicits functional magnetic resonance imaging (fMRI) activations in area LIP, but no study has yet investigated the effect of FEF microstimulation on LIP at the single-cell or local field potential (LFP) level. We recorded spiking and LFP activity in area LIP during weak, subthreshold microstimulation of the FEF in a delayed-saccade task. FEF microstimulation caused a highly time- and frequency-specific, task-dependent increase in gamma power in retinotopically corresponding sites in LIP: FEF microstimulation produced a significant increase in LIP gamma power when a saccade target appeared and remained present in the LIP receptive field (RF), whereas less specific increases in alpha power were evoked by FEF microstimulation for saccades directed away from the RF. Stimulating FEF with weak currents had no effect on LIP spike rates or on the gamma power during memory saccades or passive fixation. These results provide the first evidence for task-dependent modulations of LFPs in LIP caused by top-down stimulation of FEF. Since the allocation and disengagement of spatial attention in visual cortex have been associated with increases in gamma and alpha power, respectively, the effects of FEF microstimulation on LIP are consistent with the known effects of spatial attention.     

Response of neurons in the lateral intraparietal area to a distractor flashed during the delay period of a memory-guided saccade

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.     

Saccade-related activity in the parietal reach region

In previous experiments, we showed that cells in the parietal reach region (PRR) in monkey posterior parietal cortex code intended reaching movements in an eye-centered frame of reference. These cells are more active when an arm compared with an eye movement is being planned. Despite this clear preference for arm movements, we now report that PRR neurons also fire around the time of a saccade. Of 206 cells tested, 29% had perisaccadic activity in a delayed-saccade task. Two findings indicate that saccade-related activity does not reflect saccade planning or execution. First, activity is often peri- or postsaccadic but seldom presaccadic. Second, cells with saccade-related activity were no more likely to show strong saccadic delay period activity than cells without saccade-related activity. These findings indicate that PRR cells do not take part in saccade planning. Instead, the saccade-related activity in PRR may reflect cross-coupling between reach and saccade pathways that may be used to facilitate eye-hand coordination. Alternatively, saccade-related activity may reflect eye position information that could be used to maintain an eye-centered representation of intended reach targets across eye movements.     

The time course of perisaccadic receptive field shifts in the lateral intraparietal area of the monkey

Neurons in the lateral intraparietal area of the monkey (LIP) have visual receptive fields in retinotopic coordinates when studied in a fixation task. However, in the period immediately surrounding a saccade these receptive fields often shift, so that a briefly flashed stimulus outside the receptive field will drive the neurons if the eye movement will bring the spatial location of that vanished stimulus into the receptive field. This is equivalent to a transient shift of the retinal receptive field. The process enables the monkey brain to process a stimulus in a spatially accurate manner after a saccade, even though the stimulus appeared only before the saccade. We studied the time course of this receptive field shift by flashing a task-irrelevant stimulus for 100 ms before, during, or after a saccade. The stimulus could appear in receptive field as defined by the fixation before the saccade (the current receptive field) or the receptive field as defined by the fixation after the saccade (the future receptive field). We recorded the activity of 48 visually responsive neurons in LIP of three hemispheres of two rhesus monkeys. We studied 45 neurons in the current receptive field task, in which the saccade removed the stimulus from the receptive field. Of these neurons 29/45 (64%) showed a significant decrement of response when the stimulus appeared 250 ms or less before the saccade, as compared with their activity during fixation. The average response decrement was 38% for those cells showing a significant (P < 0.05 by t-test) decrement. We studied 39 neurons in the future receptive field task, in which the saccade brought the spatial location of a recently vanished stimulus into the receptive field. Of these 32/39 (82%) had a significant response to stimuli flashed for 100 ms in the future receptive field, even 400 ms before the saccade. Neurons never responded to stimuli moved by the saccade from a point outside the receptive field to another point outside the receptive field. Neurons did not necessarily show any saccadic suppression for stimuli moved from one part of the receptive field to another by the saccade. Stimuli flashed <250 ms before the saccade-evoked responses in both the presaccadic and the postsaccadic receptive fields, resulting in an increase in the effective receptive field size, an effect that we suggest is responsible for perisaccadic perceptual inaccuracies.     

Representation of the visual field in the lateral intraparietal area of macaque monkeys: a quantitative receptive field analysis

The representation of the visual field in the primate lateral intraparietal area (LIP) was examined, using a rapid, computer-driven receptive field (RF) mapping procedure. RF characteristics of single LIP neurons could thus be measured repeatedly under different behavioral conditions. Here we report data obtained using a standard ocular fixation task during which the animals were required to monitor small changes in color of the fixated target. In a first step, statistical analyses were conducted in order to establish the experimental limits of the mapping procedure on 171 LIP neurons recorded from three hemispheres of two macaque monkeys. The characteristics of the receptive fields of LIP neurons were analyzed at the single cell and at the population level. Although for many neurons the assumption of a simple two-dimensional gaussian profile with a central area of maximal excitability at the center and progressively decreasing response strength at the periphery can represent relatively accurately the spatial structure of the RF, about 19% of the cells had a markedly asymmetrical shape. At the population level, we observed, in agreement with prior studies, a systematic relation between RF size and eccentricity. However, we also found a more accentuated overrepresentation of the central visual field than had been previously reported and no marked differences between the upper and lower visual representation of space. This observation correlates with an extension of the definition of LIP from the posterior third of the lateral intraparietal sulcus to most of the middle and posterior thirds. Detailed histological analyses of the recorded hemispheres suggest that there exists, in this newly defined unitary functional cortical area, a coarse but systematic topographical organization in area LIP that supports the distinction between its dorsal and ventral regions, LIPd and LIPv, respectively. Paralleling the physiological data, the central visual field is mostly represented in the middle dorsal region and the visual periphery more ventral and posterior. An anteroposterior gradient from the lower to the upper visual field representations can also be identified. In conclusion, this study provides the basis for a reliable mapping method in awake monkeys and a reference for the organization of the properties of the visual space representation in an area LIP extended with respect to the previously described LIP and showing a relative emphasis of central visual field. Electronic Publication