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     

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.     

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.     

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.     

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.     

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.     

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.     

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.     

3-Dimensional eye-head coordination in gaze shifts evoked during stimulation of the lateral intraparietal cortex

Coordinated eye-head gaze shifts have been evoked during electrical stimulation of the frontal cortex (supplementary eye field (SEF) and frontal eye field (FEF)) and superior colliculus (SC), but less is known about the role of lateral intraparietal cortex (LIP) in head-unrestrained gaze shifts. To explore this, two monkeys (M1 and M2) were implanted with recording chambers and 3-D eye+ head search coils. Tungsten electrodes delivered trains of electrical pulses (usually 200 ms duration) to and around area LIP during head-unrestrained gaze fixations. A current of 200 μA consistently evoked small, short-latency contralateral gaze shifts from 152 sites in M1 and 243 sites in M2 (Constantin et al., 2007). Gaze kinematics were independent of stimulus amplitude and duration, except that subsequent saccades were suppressed. The average amplitude of the evoked gaze shifts was 8.46° for M1 and 8.25° for M2, with average head components of only 0.36 and 0.62° respectively. The head's amplitude contribution to these movements was significantly smaller than in normal gaze shifts, and did not increase with behavioral adaptation. Stimulation-evoked gaze, eye and head movements qualitatively obeyed normal 3-D constraints (Donders' law and Listing's law), but with less precision. As in normal behavior, when the head was restrained LIP stimulation evoked eye-only saccades in Listing's plane, whereas when the head was not restrained, stimulation evoked saccades with position-dependent torsional components (driving the eye out of Listing's plane). In behavioral gaze-shifts, the vestibuloocular reflex (VOR) then drives torsion back into Listing's plane, but in the absence of subsequent head movement the stimulation-induced torsion was “left hanging”. This suggests that the position-dependent torsional saccade components are preprogrammed, and that the oculomotor system was expecting a head movement command to follow the saccade. These data show that, unlike SEF, FEF, and SC stimulation in nearly identical conditions, LIP stimulation fails to produce normally-coordinated eye-head gaze shifts.     

Functional and histological properties of caudal intraparietal area of macaque monkey

In our previous studies, we found that cells in the caudal intraparietal (CIP) area of the macaque monkey selectively responded to three-dimensional (3D) features, such as the axis and surface orientations, and we suggested that this area played a crucial role in 3D vision. In this study, we investigated (1) whether cells in CIP respond to other 3D features, such as curvature, and (2) whether CIP has any histological property to distinguish it from neighboring areas. Curvatures defined by a random-dot stereogram were presented on a display while the monkey performed a fixation task. The shape and amount of curvature were manipulated by two independent variables, shape index and curvedness, respectively. Two-way ANOVA showed that 19 out of 56 visually responsive cells (34.0%) showed the main effect of shape index. We tentatively designated these cells as 3D curvature-selective (3DCS). Of these, six 3DCS cells showed the main effects of shape index and curvedness, whereas 13 showed the main effect of shape index only. In both types of 3DCS cells, preferred shape indices calculated from tuning curves at two levels of curvedness matched well. These results indicate that the majority of 3DCS cells responded equally to a particular shape of curvatures with different curvedness levels. An immunohistochemical study showed that the recording sites of 3DCS cells were in a cortical region characterized by a dense SMI-32 immunoreactivity in the caudal portion of the lateral intraparietal sulcus (IPS), which suggests that this region is comparable to the lateral occipital parietal (LOP) designated in the caudal IPS previously. Further investigations showed that this region was separated from LIPv, the ventral subdivision of lateral intraparietal (LIP) located rostral to CIP/LOP. These results suggest that CIP is a cortical area distinct from LIP histologically as well as functionally.     

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)     

Magnification factor and receptive field size in foveal striate cortex of the monkey

Summary Receptive field size and magnification have been studied in striate cortex of awake, behaving rhesus monkeys at visual eccentricities in the range of 5–160 min. The major findings that emerge are (1) magnification in the foveola achieves values in the range of 30 mm/deg, (2) mean field size is not proportional to inverse magnification in contrast with previous reports, and (3) the product, magnification X aggregate field size, is greater in central vision than in peripheral vision. Thus, a point of light projected onto foveal retina is seen by larger numbers of striate cortical cells than a point of light projected onto peripheral retina.Implications of these findings for visual localization and two-point discrimination are discussed.Dedicated to Hermann RahnSupported by NIH grants EY02349 and 5 T32 EY07019     

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.     

Dynamic shifts of visual receptive fields in cortical area MT by spatial attention

Voluntary attention is the top-down selection process that focuses cortical processing resources on the most relevant sensory information. Spatial attention--that is, selection based on stimulus position--alters neuronal responsiveness throughout primate visual cortex. It has been hypothesized that it also changes receptive field profiles by shifting their centers toward attended locations and by shrinking them around attended stimuli. Here we examined, at high resolution, receptive fields in cortical area MT of rhesus macaque monkeys when their attention was directed to different locations within and outside these receptive fields. We found a shift of receptive fields, even far from the current location of attention, accompanied by a small amount of shrinkage. Thus, already in early extrastriate cortex, receptive fields are not static entities but are highly modifiable, enabling the dynamic allocation of processing resources to attended locations and supporting enhanced perception within the focus of attention by effectively increasing the local cortical magnification.     

Second-order receptive fields reveal multidigit interactions in area 3b of the macaque monkey

Linear receptive field (RF) models of area 3b neurons reveal a three-component structure: a central excitatory region flanked by two inhibitory regions that are spatially and temporally nonoverlapping with the excitation. Previous studies also report that there is an "infield" inhibitory region throughout the neuronal RF, which is a nonlinear interactive (second order) effect whereby stimuli lagging an input to the excitatory region are suppressed. Thus linear models may be inaccurate approximations of the neurons' true RFs. In this study, we characterize the RFs of area 3b neurons, using a second-order quadratic model. Data were collected from 80 neurons of two awake, behaving macaque monkeys while a random dot pattern was scanned simultaneously across the distal pads of digits D2, 3, and 4. We used an iterative method derived from matching pursuit to identify a set of linear and nonlinear terms with significant effects on the neuronal response. For most neurons (65/80), the linear component of the quadratic RF was characterized by a single excitatory region on the dominant digit. Interactions within the dominant digit were characterized by two quadratic filters that capture the spatial aspects of the interactive infield inhibition. Interactions between the dominant (most responsive) digit and its adjacent digit(s) formed the largest class of cross-digit interactions. The results demonstrate that a significant part of area 3b responses is due to nonlinear mechanisms, and furthermore, the data support the notion that area 3b neurons have "nonclassical RF"-like input from adjacent fingers, indicating that area 3b plays a role in integrating shape inputs across digits.     

Effect of reversible inactivation of macaque lateral intraparietal area on visual and memory saccades

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.