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°. 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.

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Visuopathy of prematurity: is retinopathy just the tip of the iceberg?

Pediatric Research ◽

10.1038/s41390-021-01625-0 ◽

2021 ◽

Author(s):

Sigrid Hegna Ingvaldsen ◽

Tora Sund Morken ◽

Dordi Austeng ◽

Olaf Dammann

Keyword(s):

Visual Processing ◽

Structural Changes ◽

Developmental Trajectories ◽

Visual Pathway ◽

Visual Stream ◽

Visual Deficits ◽

Cortical Areas ◽

Cellular Architecture ◽

Increased Risk ◽

Dorsal Visual Stream

AbstractResearch on retinopathy of prematurity (ROP) focuses mainly on the abnormal vascularization patterns that are directly visible for ophthalmologists. However, recent findings indicate that children born prematurely also exhibit changes in the retinal cellular architecture and along the dorsal visual stream, such as structural changes between and within cortical areas. Moreover, perinatal sustained systemic inflammation (SSI) is associated with an increased risk for ROP and the visual deficits that follow. In this paper, we propose that ROP might just be the tip of an iceberg we call visuopathy of prematurity (VOP). The VOP paradigm comprises abnormal vascularization of the retina, alterations in retinal cellular architecture, choroidal degeneration, and abnormalities in the visual pathway, including cortical areas. Furthermore, VOP itself might influence the developmental trajectories of cerebral structures and functions deemed responsible for visual processing, thereby explaining visual deficits among children born preterm.

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The Effect of FEF Microstimulation on the Responses of Neurons in the Lateral Intraparietal Area

Journal of Cognitive Neuroscience ◽

10.1162/jocn_a_00591 ◽

2014 ◽

Vol 26 (8) ◽

pp. 1672-1684 ◽

Cited By ~ 2

Author(s):

Elsie Premereur ◽

Wim Vanduffel ◽

Peter Janssen

Keyword(s):

Receptive Field ◽

Direct Evidence ◽

Spike Rate ◽

Visually Guided ◽

Lateral Intraparietal Area ◽

Oculomotor Behavior ◽

Cortical Areas ◽

Gamma Power ◽

Saccade Task ◽

High Level

The macaque FEFs and the lateral intraparietal area (LIP) are high-level cortical areas involved in both spatial attention and oculomotor behavior. Stimulating FEF at a level below the threshold for evoking saccades increases fMRI activity and gamma power in area LIP, but the precise effect exerted by the FEF on LIP neurons is unknown. In our study, we recorded LIP single-unit activity during a visually guided saccade task with a peripherally presented go signal during microstimulation of FEF. We found that FEF microstimulation increased the LIP spike rate immediately after the highly salient go signal inside the LIP receptive field when both target and go signal were presented inside the receptive field, and no other possible go cues were present on the screen. The effect of FEF microstimulation on the LIP response was positive until at least 800 msec after microstimulation had ceased, but reversed for longer trial durations. Therefore, FEF microstimulation can modulate the LIP spike rate only when attention is selectively directed toward the stimulated location. These results provide the first direct evidence for LIP spike rate modulations caused by FEF microstimulation, thus showing that FEF activity can be the source of top–down control of area LIP.

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Grasping Execution and Grasping Observation Activity of Single Neurons in the Macaque Anterior Intraparietal Area

Journal of Cognitive Neuroscience ◽

10.1162/jocn_a_00647 ◽

2014 ◽

Vol 26 (10) ◽

pp. 2342-2355 ◽

Cited By ~ 43

Author(s):

Pierpaolo Pani ◽

Tom Theys ◽

Maria C. Romero ◽

Peter Janssen

Keyword(s):

Visual Field ◽

Premotor Cortex ◽

Visually Guided ◽

Simple Shape ◽

Visual Stream ◽

Cortical Areas ◽

Person Perspective ◽

First Person Perspective ◽

Dorsal Visual Stream ◽

Passive Fixation

Primates use vision to guide their actions in everyday life. Visually guided object grasping is known to rely on a network of cortical areas located in the parietal and premotor cortex. We recorded in the anterior intraparietal area (AIP), an area in the dorsal visual stream that is critical for object grasping and densely connected with the premotor cortex, while monkeys were grasping objects under visual guidance and during passive fixation of videos of grasping actions from the first-person perspective. All AIP neurons in this study responded during grasping execution in the light, that is, became more active after the hand had started to move toward the object and during grasping in the dark. More than half of these AIP neurons responded during the observation of a video of the same grasping actions on a display. Furthermore, these AIP neurons responded as strongly during passive fixation of movements of a hand on a scrambled background and to a lesser extent to a shape appearing within the visual field near the object. Therefore, AIP neurons responding during grasping execution also respond during passive observation of grasping actions and most of them even during passive observation of movements of a simple shape in the visual field.

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Responses of Ventral Posterior Thalamus Neurons to Three-Dimensional Vestibular and Optic Flow Stimulation

Journal of Neurophysiology ◽

10.1152/jn.00729.2009 ◽

2010 ◽

Vol 103 (2) ◽

pp. 817-826 ◽

Cited By ~ 20

Author(s):

Hui Meng ◽

Dora E. Angelaki

Keyword(s):

Optic Flow ◽

Visual Motion ◽

Three Dimensional ◽

Cerebellar Nuclei ◽

Visual Stream ◽

Posterior Thalamus ◽

Cortical Areas ◽

3D Space ◽

Flow Stimulation ◽

Dorsal Visual Stream

Multisensory neurons tuned to both vestibular and visual motion (optic flow) signals are found in several cortical areas in the dorsal visual stream. Here we examine whether such convergence occurs subcortically in the macaque thalamus. We searched the ventral posterior nuclei, including the anterior pulvinar, as well as the ventro-lateral and ventral posterior lateral nuclei, areas that receive vestibular signals from brain stem and deep cerebellar nuclei. Approximately a quarter of cells responded to three-dimensional (3D) translational and/or rotational motion. More than half of the responsive cells were convergent, thus responded during both rotation and translation. The preferred axes of translation/rotation were distributed throughout 3D space. The majority of the neurons were excited, but some were inhibited, during rotation/translation in darkness. Only a couple of neurons were multisensory being tuned to both vestibular and optic flow stimuli. We conclude that multisensory vestibular/optic flow neurons, which are commonly found in cortical visual and visuomotor areas, are rare in the ventral posterior thalamus.

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Comparison of Cortico-Cortical and Cortico-Collicular Signals for the Generation of Saccadic Eye Movements

Journal of Neurophysiology ◽

10.1152/jn.00317.2001 ◽

2002 ◽

Vol 87 (2) ◽

pp. 845-858 ◽

Cited By ~ 100

Author(s):

Stefano Ferraina ◽

Martin Paré ◽

Robert H. Wurtz

Keyword(s):

Cerebral Cortex ◽

Eye Movements ◽

Visual Processing ◽

Full Range ◽

Saccadic Eye Movements ◽

Projection Neurons ◽

Visual Response ◽

Antidromic Activation ◽

Cortical Areas ◽

Saccade Task

Many neurons in the frontal eye field (FEF) and lateral intraparietal (LIP) areas of cerebral cortex are active during the visual-motor events preceding the initiation of saccadic eye movements: they respond to visual targets, increase their activity before saccades, and maintain their activity during intervening delay periods. Previous experiments have shown that the output neurons from both LIP and FEF convey the full range of these activities to the superior colliculus (SC) in the brain stem. These areas of cerebral cortex also have strong interconnections, but what signals they convey remains unknown. To determine what these cortico-cortical signals are, we identified the LIP neurons that project to FEF by antidromic activation, and we studied their activity during a delayed-saccade task. We then compared these cortico-cortical signals to those sent subcortically by also identifying the LIP neurons that project to the intermediate layers of the SC. Of 329 FEF projection neurons and 120 SC projection neurons, none were co-activated by both FEF and SC stimulation. FEF projection neurons were encountered more superficially in LIP than SC projection neurons, which is consistent with the anatomical projection of many cortical layer III neurons to other cortical areas and of layer V neurons to subcortical structures. The estimated conduction velocities of FEF projection neurons (16.7 m/s) were significantly slower that those of SC projection neurons (21.7 m/s), indicating that FEF projection neurons have smaller axons. We identified three main differences in the discharge properties of FEF and SC projection neurons: only 44% of the FEF projection neurons changed their activity during the delayed-saccade task compared with 69% of the SC projection neurons; only 17% of the task-related FEF projection neurons showed saccadic activity, whereas 42% of the SC projection neurons showed such increases; 78% of the FEF projection neurons had a visual response but no saccadic activity, whereas only 55% of the SC projection neurons had similar activity. The FEF and SC projection neurons had three similarities: both had visual, delay, and saccadic activity, both had stronger delay and saccadic activity with visually guided than with memory-guided saccades, and both had broadly tuned responses for disparity stimuli, suggesting that their visual receptive fields have a three-dimensional configuration. These observations indicate that the activity carried between parietal and frontal cortical areas conveys a spectrum of signals but that the preponderance of activity conveyed might be more closely related to earlier visual processing than to the later saccadic stages that are directed to the SC.

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Saccade-related activity in the lateral intraparietal area. I. Temporal properties; comparison with area 7a

Journal of Neurophysiology ◽

10.1152/jn.1991.66.3.1095 ◽

1991 ◽

Vol 66 (3) ◽

pp. 1095-1108 ◽

Cited By ~ 271

Author(s):

S. Barash ◽

R. M. Bracewell ◽

L. Fogassi ◽

J. W. Gnadt ◽

R. A. Andersen

Keyword(s):

Time Course ◽

Activity Index ◽

Saccadic Eye Movements ◽

Background Level ◽

Companion Paper ◽

S Phase ◽

Activity Levels ◽

Lateral Intraparietal Area ◽

Area 7A ◽

Saccade Task

1. The cortex of the inferior parietal lobule (IPL) contains neurons whose activity is related to saccadic eye movements. The exact role of the IPL in relation to saccades remains, however, unclear. In this and the companion paper, we approach this problem by quantifying many of the spatial and temporal parameters of the saccade-related (S) activity. These parameters have hitherto been largely unstudied. 2. The activity of single neurons was recorded from Macaca mulatta monkeys while they were performing a delayed-saccade task. The analysis presented here is based on 161 neurons recorded from the lateral intraparietal area (LIP), a recently defined subdivision of the IPL; and 54 neurons recorded from the neighboring part of the IPL, area 7a. Overall, 409 IPL neurons were isolated in this study. 3. The typical activity of IPL neurons during the delayed-saccade task has three basic phases: light sensitive (LS), memory (M), and S. These basic phases are common to neurons of both areas LIP and 7a. In each phase (LS, M, and S), individual neurons may or may not be active. Most LIP neurons, however, are active in more than one phase. 4. To compare the activity levels of different neurons, the actual firing rate was weighted by each neuron's background level, yielding an "activity index" for each neuron, in each phase of the task. We calculated the activity index for the LS and M phases and for three phases related to the saccade: a presaccadic (Pre-S), a saccade-coincident (S-Co), and a postsaccadic (Post-S) phase. For area LIP neurons the median values of the activity index were high for the LS, M, Pre-S, and S-Co activities, and slightly lower in the Post-S period. In area 7a the median values were low for the LS phase and, in particular, for the M and Pre-S phases, somewhat higher coincident with the saccade, and high post-saccadically. 5. In area LIP, in each phase, 49-63% of the neurons had excitatory activity, and 10-17% had inhibitory responses. 6. In contrast, in area 7a excitatory responses were most frequent in the Post-S phase (56%). Excitation was particularly infrequent during M (28%) and Pre-S (22%). The incidence of inhibitory responses varied too (4-18%). The time course of inhibition was roughly opposite that of excitation; the highest frequency of inhibitory responses occurred during the saccade.(ABSTRACT TRUNCATED AT 400 WORDS)

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Motor intention activity in the macaque's lateral intraparietal area. I. Dissociation of motor plan from sensory memory

Journal of Neurophysiology ◽

10.1152/jn.1996.76.3.1439 ◽

1996 ◽

Vol 76 (3) ◽

pp. 1439-1456 ◽

Cited By ~ 126

Author(s):

P. Mazzoni ◽

R. M. Bracewell ◽

S. Barash ◽

R. A. Andersen

Keyword(s):

Eye Movements ◽

Visual Stimulus ◽

Visual Stimuli ◽

Saccadic Eye Movements ◽

Stimulus Location ◽

Sensory Memory ◽

Lateral Intraparietal Area ◽

Preferred Direction ◽

Motor Plan ◽

Stimulation Of

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

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A spatial memory signal shows that the parietal cortex has access to a craniotopic representation of space

eLife ◽

10.7554/elife.30762 ◽

2018 ◽

Vol 7 ◽

Cited By ~ 3

Author(s):

Mulugeta Semework ◽

Sara C Steenrod ◽

Michael E Goldberg

Keyword(s):

Spatial Memory ◽

Parietal Cortex ◽

Receptive Fields ◽

Spatial Location ◽

Visual Response ◽

Lateral Intraparietal Area ◽

Memory Response ◽

Representation Of Space ◽

Present Trial

Humans effortlessly establish a gist-like memory of their environment whenever they enter a new place, a memory that can guide action even in the absence of vision. Neurons in the lateral intraparietal area (LIP) of the monkey exhibit a form of this environmental memory. These neurons respond when a monkey makes a saccade that brings the spatial location of a stimulus that appeared on a number of prior trials, but not on the present trial, into their receptive fields (RFs). The stimulus need never have appeared in the neuron’s RF. This memory response is usually weaker, with a longer latency than the neuron’s visual response. We suggest that these results demonstrate that LIP has access to a supraretinal memory of space, which is activated when the spatial location of the vanished stimulus can be described by a retinotopic vector from the center of gaze to the remembered spatial location.

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