investigating-object-representations-macaque-dorsal-visual-stream

Investigating Object Representations in the Macaque Dorsal Visual Stream Using Single-unit Recordings

Previous studies have shown that neurons in parieto-frontal areas of the macaque brain can be highly selective for real-world objects, disparity-defined ...

Katholieke Universiteit Leuven

The Leuven Brain Institute

The analysis of object shape is critical for both object recognition and grasping. Areas in the intraparietal sulcus of the rhesus monkey are important for the visuomotor transformations underlying actions directed toward objects. The lateral intraparietal (LIP) area has strong anatomical connections with the anterior intraparietal area, which is known to control the shaping of the hand during grasping, and LIP neurons can respond selectively to simple two-dimensional shapes. Here we investigate the shape representation in area LIP of awake rhesus monkeys. Specifically, we determined to what extent LIP neurons are tuned to shape dimensions known to be relevant for grasping and assessed the invariance of their shape preferences with regard to changes in stimulus size and position in the receptive field. Most LIP neurons proved to be significantly tuned to multiple shape dimensions. The population of LIP neurons that were tested showed barely significant size invariance. Position invariance was present in a minority of the neurons tested. Many LIP neurons displayed spurious shape selectivity arising from accidental interactions between the stimulus and the receptive field. We observed pronounced differences in the receptive field profiles determined by presenting two different shapes. Almost all LIP neurons showed spatially selective saccadic activity, but the receptive field for saccades did not always correspond to the receptive field as determined using shapes. Our results demonstrate that a subpopulation of LIP neurons encodes stimulus shape. Furthermore, the shape representation in the dorsal visual stream appears to differ radically from the known representation of shape in the ventral visual stream.

Coding of shape and position in macaque lateral intraparietal area.

Differences in the horizontal positions of retinal images--binocular disparity--provide important cues for three-dimensional object recognition and manipulation. We investigated the neural coding of three-dimensional shape defined by disparity in anterior intraparietal (AIP) area. Robust selectivity for disparity-defined slanted and curved surfaces was observed in a high proportion of AIP neurons, emerging at relatively short latencies. The large majority of AIP neurons preserved their three-dimensional shape preference over different positions in depth, a hallmark of higher-order disparity selectivity. Yet both stimulus type (concave-convex) and position in depth could be reliably decoded from the AIP responses. The neural coding of three-dimensional shape was based on first-order (slanted surfaces) and second-order (curved surfaces) disparity selectivity. Many AIP neurons tolerated the presence of disparity discontinuities in the stimulus, but the population of AIP neurons provided reliable information on the degree of curvedness of the stimulus. Finally, AIP neurons preserved their three-dimensional shape preference over different positions in the frontoparallel plane. Thus, AIP neurons extract or have access to three-dimensional object information defined by binocular disparity, consistent with previous functional magnetic resonance imaging data. Unlike the known representation of three-dimensional shape in inferior temporal cortex, the neural representation in AIP appears to emphasize object parameters required for the planning of grasping movements.

A distinct representation of three-dimensional shape in macaque anterior intraparietal area: fast, metric, and coarse.

We have developed three fluorine-18 labeled 6-(methyl)amino-2-(4'-fluorophenyl)-1,3-benzothiazoles, which display high in vitro binding affinity for human amyloid beta plaques (K(i) < or = 10 nM). The radiolabeled probes were synthesized by aromatic nucleophilic substitution of the corresponding nitro precursor with (18)F-fluoride, followed by deprotection of the BOC group if required. Determination of the octanol/water partition coefficient, biodistribution studies in mice, and in vivo muPET studies in rats and a rhesus monkey showed that initial brain uptake was high and brain washout was fast in normal animals. Radiometabolites were quantified in plasma and brain of mice and in monkey plasma using HPLC. Of the tested compounds, [(18)F]2 (6-amino-2-(4'-[(18)F]fluorophenyl)-1,3-benzothiazole) shows the most favorable brain kinetics in mice, rats, and a monkey. Its polar plasma radiometabolites do not cross the blood-brain barrier. The preliminary results strongly suggest that this new fluorinated compound is a promising candidate as a PET brain amyloid imaging agent.

Synthesis and evaluation of three 18F-labeled aminophenylbenzothiazoles as amyloid imaging agents.

The macaque lateral intraparietal area (LIP) has been implicated in many cognitive processes, ranging from saccade planning and spatial attention to timing and categorization. Importantly, different research groups have used different criteria for including LIP neurons in their studies. While some research groups have selected LIP neurons based on the presence of memory-delay activity, other research groups have used other criteria such as visual, presaccadic, and/or memory activity. We recorded from LIP neurons that were selected based on spatially selective saccadic activity but regardless of memory-delay activity in macaque monkeys. To test anticipatory climbing activity, we used a delayed visually guided saccade task with a unimodal schedule of go-times, for which the conditional probability that the go-signal will occur rises monotonically as a function of time. A subpopulation of LIP neurons showed anticipatory activity that mimicked the subjective hazard rate of the go-signal when the animal was planning a saccade toward the receptive field. A large subgroup of LIP neurons, however, did not modulate their firing rates according to the subjective hazard function. These non-anticipatory neurons were strongly influenced by salient visual stimuli appearing in their receptive field, but less so by the direction of the impending saccade. Thus, LIP contains a heterogeneous population of neurons related to saccade planning or visual salience, and these neurons are spatially intermixed. Our results suggest that between-study differences in neuronal selection may have contributed significantly to the findings of different research groups with respect to the functional role of area LIP.

Functional heterogeneity of macaque lateral intraparietal neurons.

The macaque anterior intraparietal area (AIP) is crucial for visually guided grasping. AIP neurons respond during the visual presentation of real-world objects and encode the depth profile of disparity-defined curved surfaces. We investigated the neural representation of curved surfaces in AIP using a stimulus-reduction approach. The stimuli consisted of three-dimensional (3-D) shapes curved along the horizontal axis, the vertical axis, or both the horizontal and the vertical axes of the shape. The depth profile was defined solely by binocular disparity that varied along either the boundary or the surface of the shape or along both the boundary and the surface of the shape. The majority of AIP neurons were selective for curved boundaries along the horizontal or the vertical axis, and neural selectivity emerged at short latencies. Stimuli in which disparity varied only along the surface of the shape (with zero disparity on the boundaries) evoked selectivity in a smaller proportion of AIP neurons and at considerably longer latencies. AIP neurons were not selective for 3-D surfaces composed of anticorrelated disparities. Thus the neural selectivity for object depth profile in AIP is present when only the boundary is curved in depth, but not for disparity in anticorrelated stereograms.

Selectivity for three-dimensional contours and surfaces in the anterior intraparietal area.

Oscillatory brain activity is attracting increasing interest in cognitive neuroscience. Numerous EEG (magnetoencephalography) and local field potential (LFP) measurements have related cognitive functions to different types of brain oscillations, but the functional significance of these rhythms remains poorly understood. Despite its proven value, LFP activity has not been extensively tested in the macaque lateral intraparietal area (LIP), which has been implicated in a wide variety of cognitive control processes. We recorded action potentials and LFPs in area LIP during delayed eye movement tasks and during a passive fixation task, in which the time schedule was fixed so that temporal expectations about task-relevant cues could be formed. LFP responses in the gamma band discriminated reliably between saccade targets and distractors inside the receptive field (RF). Alpha and beta responses were much less strongly affected by the presence of a saccade target, however, but rose sharply in the waiting period before the go signal. Surprisingly, conditions without visual stimulation of the LIP-RF-evoked robust LFP responses in every frequency band--most prominently in those below 50 Hz--precisely time-locked to the expected time of stimulus onset in the RF. These results indicate that in area LIP, oscillations in the LFP, which reflect synaptic input and local network activity, are tightly coupled to the temporal expectation of task-relevant cues.

Local field potential activity associated with temporal expectations in the macaque lateral intraparietal area.

Neurons in the macaque dorsal visual stream respond to the visual presentation of objects in the context of a grasping task and to three-dimensional (3D) surfaces defined by binocular disparity, but little is known about the neural representation of two-dimensional (2D) shape in the dorsal stream. We recorded the activity of single neurons in the macaque anterior intraparietal area (AIP), which is known to be crucial for grasping, during the presentation of images of objects and silhouette, outline and line-drawing versions of these images (contour stimuli). The vast majority of AIP neurons responding selectively to 2D images were also selective for at least one of the contour stimuli with the same boundary shape, suggesting that the boundary is sufficient for the image selectivity of most AIP neurons. Furthermore, a subset of these neurons with foveal receptive fields generally preserved the shape preference across positions, whereas for more than half of the AIP population the center of the receptive field was at a parafoveal location with less tolerance to changes in stimulus position. AIP neurons frequently exhibited shape selectivity across different stimulus sizes. These results demonstrate that AIP neurons encode not only 3D but also 2D shape features.

Responses to two-dimensional shapes in the macaque anterior 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.

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

Anatomical studies indicate that area F5 in the macaque ventral premotor cortex consists of three different sectors. One of these is F5a in the posterior bank of the inferior arcuate sulcus, but no functional characterization of F5a at the single-cell level exists. We investigated the neuronal selectivity for three-dimensional (3D) shape and grasping activity in F5a. In contrast to neighboring regions F5p and 45B, the great majority of F5a neurons showed selectivity for disparity-defined curved surfaces, and most neurons preserved this selectivity across positions in depth, indicating higher-order disparity selectivity. Thus, as predicted by monkey fMRI data, F5a neurons showed robust 3D-shape selectivity in the absence of a motor response. To investigate the relationship between disparity selectivity and grasping activity, we recorded from 3D-shape-selective F5a neurons during a visually guided grasping task and during grasping in the dark. F5a neurons encoding the depth profile of curved surfaces frequently responded during grasping of real-world objects in the light, but not in the dark, whereas nearby neurons were also active in the dark. The presence of 3D-shape-selective and "visual-dominant" neurons demonstrates that the F5a sector is distinct from neighboring regions of ventral premotor cortex, in line with recent anatomical connectivity studies.

Selectivity for three-dimensional shape and grasping-related activity in the macaque ventral premotor cortex.

The exquisite ability of primates to grasp and manipulate objects relies on the transformation of visual information into motor commands. To this end, the visual system extracts object affordances that can be used to program and execute the appropriate grip. The macaque anterior intraparietal (AIP) area has been implicated in the extraction of affordances for the purpose of grasping. Neurons in the AIP area respond during visually guided grasping and to the visual presentation of objects. A subset of AIP neurons is also activated by two-dimensional images of objects and even by outline contours defining the object shape, but it is unknown how AIP neurons actually represent object shape. In this study, we used a stimulus reduction approach to determine the minimum effective shape feature evoking AIP responses. AIP neurons responding to outline shapes also responded selectively to very small fragment stimuli measuring only 1-2°. This fragment selectivity could not be explained by differences in eye movements or simple orientation selectivity, but proved to be highly dependent on the relative position of the stimulus in the receptive field. Our findings challenge the current understanding of the AIP area as a critical stage in the dorsal stream for the extraction of object affordances. 

Coding of shape features in the macaque anterior intraparietal area.

The primate visual system extracts object shape information for object recognition in the ventral visual stream. Recent research has demonstrated that object shape is also processed in the dorsal visual stream, which is specialized for spatial vision and the planning of actions. A number of studies have investigated the coding of 2D shape in the anterior intraparietal area (AIP), one of the end-stage areas of the dorsal stream which has been implicated in the extraction of affordances for the purpose of grasping. These findings challenge the current understanding of area AIP as a critical stage in the dorsal stream for the extraction of object affordances. The representation of three-dimensional (3D) shape has been studied in two interconnected areas known to be critical for object grasping: area AIP and area F5a in the ventral premotor cortex (PMv), to which AIP projects. In both areas neurons respond selectively to 3D shape defined by binocular disparity, but the latency of the neural selectivity is approximately 10 ms longer in F5a compared to AIP, consistent with its higher position in the hierarchy of cortical areas. Furthermore, F5a neurons were more sensitive to small amplitudes of 3D curvature and could detect subtle differences in 3D structure more reliably than AIP neurons. In both areas, 3D-shape selective neurons were co-localized with neurons showing motor-related activity during object grasping in the dark, indicating a close convergence of visual and motor information on the same clusters of neurons. 

Shape representations in the primate dorsal visual stream.

The division of labor between the dorsal and the ventral visual stream in the primate brain has inspired numerous studies on the visual system in humans and in nonhuman primates. However, how and under which circumstances the two visual streams interact is still poorly understood. Here we review evidence from anatomy, modelling, electrophysiology, electrical microstimulation (EM), reversible inactivation and functional imaging in the macaque monkey aimed at clarifying at which levels in the hierarchy of visual areas the two streams interact, and what type of information might be exchanged between the two streams during three-dimensional (3D) object viewing. Neurons in both streams encode 3D structure from binocular disparity, synchronized activity between parietal and inferotemporal areas is present during 3D structure categorization, and clusters of 3D structure-selective neurons in parietal cortex are anatomically connected to ventral stream areas. In addition, caudal intraparietal cortex exerts a causal influence on 3D-structure related activations in more anterior parietal cortex and in inferotemporal cortex. Thus, both anatomical and functional evidence indicates that the dorsal and the ventral visual stream interact during 3D object viewing.

Functional interactions between the macaque dorsal and ventral visual pathways during three-dimensional object vision.

The cortical network processing three-dimensional (3D) object structure defined by binocular disparity spans both the ventral and dorsal visual streams. However, very little is known about the neural representation of 3D structure at intermediate levels of the visual hierarchy. Here, we investigated the neural selectivity for 3D surfaces in the macaque Posterior Intraparietal area (PIP) in the medial bank of the caudal intraparietal sulcus (IPS). We first identified a region sensitive to depth-structure information in the medial bank of the caudal IPS using functional Magnetic Resonance Imaging (fMRI), and then recorded single-cell activity within this fMRI activation in the same animals. Most PIP neurons were selective for the 3D orientation of planar surfaces (first-order disparity) at very short latencies, whereas a very small fraction of PIP neurons were selective for curved surfaces (second-order disparity). A linear support vector machine classifier could reliably identify the direction of the disparity gradient in planar and curved surfaces based on the responses of a population of disparity-selective PIP neurons. These results provide the first detailed account of the neuronal properties in area PIP, which occupies an intermediate position in the hierarchy of visual areas involved in processing depth structure from disparity.

Caudal Intraparietal Sulcus and three-dimensional vision: A combined functional magnetic resonance imaging and single-cell study.

The primate dorsal visual stream processes object shape to guide actions involving an object, but the transmission of shape information beyond posterior parietal cortex remains largely unknown. To clarify the information flow between parietal and frontal cortex, we applied electrical microstimulation during functional Magnetic Resonance Imaging (fMRI) in a shape-selective patch in the posterior part of the Anterior Intraparietal area (pAIP) to chart its connectivity. Subsequently, we recorded single-unit responses to images of objects in the fMRI activation in prefrontal cortex, corresponding to area 45B, elicited by pAIP microstimulation. Neurons in area 45B had properties similar to neurons in pAIP, responding selectively to shape contours and to very small shape fragments measuring less than one deg at exceedingly short latencies. However, contrary to the prevailing view on the hierarchical organization of cortical areas, neurons in area 45B preferred even smaller shape fragments and had smaller receptive fields than neurons in pAIP. These findings provide the first evidence for ultra-fast shape processing in prefrontal cortex, and suggest that the pathway from pAIP to area 45B may not be important for object grasping.

Article	Year
Coding of shape and position in macaque lateral intraparietal area. The Journal of neuroscience : the official journal of the Society for Neuroscience\| PubMed ID: 18579742	2008
A distinct representation of three-dimensional shape in macaque anterior intraparietal area: fast, metric, and coarse. The Journal of neuroscience : the official journal of the Society for Neuroscience\| PubMed ID: 19710314	2009
Synthesis and evaluation of three 18F-labeled aminophenylbenzothiazoles as amyloid imaging agents. Journal of medicinal chemistry\| PubMed ID: 19877643	2009
Functional heterogeneity of macaque lateral intraparietal neurons. The Journal of neuroscience : the official journal of the Society for Neuroscience\| PubMed ID: 21865473	2011
Selectivity for three-dimensional contours and surfaces in the anterior intraparietal area. Journal of neurophysiology\| PubMed ID: 22090458	2012
Local field potential activity associated with temporal expectations in the macaque lateral intraparietal area. Journal of cognitive neuroscience\| PubMed ID: 22390466	2012
Responses to two-dimensional shapes in the macaque anterior intraparietal area. The European journal of neuroscience\| PubMed ID: 22626006	2012
Frontal eye field microstimulation induces task-dependent gamma oscillations in the lateral intraparietal area. Journal of neurophysiology\| PubMed ID: 22673327	2012
Selectivity for three-dimensional shape and grasping-related activity in the macaque ventral premotor cortex. The Journal of neuroscience : the official journal of the Society for Neuroscience\| PubMed ID: 22933788	2012
Coding of shape features in the macaque anterior intraparietal area. The Journal of neuroscience : the official journal of the Society for Neuroscience\| PubMed ID: 24623778	2014
Shape representations in the primate dorsal visual stream. Frontiers in computational neuroscience\| PubMed ID: 25954189	2015
Functional interactions between the macaque dorsal and ventral visual pathways during three-dimensional object vision. Cortex; a journal devoted to the study of the nervous system and behavior\| PubMed ID: 28258716	2018
Caudal Intraparietal Sulcus and three-dimensional vision: A combined functional magnetic resonance imaging and single-cell study. NeuroImage\| PubMed ID: 29080712	2018
Shape responses in a macaque frontal area connected to posterior parietal cortex. NeuroImage\| PubMed ID: 29920377	2018

Peter Janssen

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