Robust Coding of Eye Position in Posterior Parietal Cortex despite Context-Dependent Tuning.

Neurons in posterior parietal cortex (PPC) encode many aspects of the sensory world (e.g., scene structure), the posture of the body, and plans for action. For a downstream computation, however, only some of these dimensions are relevant; the rest are "nuisance variables" because their influence on neural activity changes with sensory and behavioral context, potentially corrupting the read-out of relevant information. Here we show that a key postural variable for vision (eye position) is represented robustly in male macaque PPC across a range of contexts, although the tuning of single neurons depended strongly on context. Contexts were defined by different stages of a visually guided reaching task, including (1) a visually sparse epoch, (2) a visually rich epoch, (3) a "go" epoch in which the reach was cued, and (4) during the reach itself. Eye position was constant within trials but varied across trials in a 3 × 3 grid spanning 24° × 24°. Using demixed principal component analysis of neural spike-counts, we found that the subspace of the population response encoding eye position is orthogonal to that encoding task context. Accordingly, a context-naive (fixed-parameter) decoder was nevertheless able to estimate eye position reliably across contexts. Errors were small given the sample size (∼1.78°) and would likely be even smaller with larger populations. Moreover, they were comparable to that of decoders that were optimized for each context. Our results suggest that population codes in PPC shield encoded signals from crosstalk to support robust sensorimotor transformations across contexts.SIGNIFICANCE STATEMENT Neurons in posterior parietal cortex (PPC) which are sensitive to gaze direction are thought to play a key role in spatial perception and behavior (e.g., reaching, navigation), and provide a potential substrate for brain-controlled prosthetics. Many, however, change their tuning under different sensory and behavioral contexts, raising the prospect that they provide unreliable representations of egocentric space. Here, we analyze the structure of encoding dimensions for gaze direction and context in PPC during different stages of a visually guided reaching task. We use demixed dimensionality reduction and decoding techniques to show that the coding of gaze direction in PPC is mostly invariant to context. This suggests that PPC can provide reliable spatial information across sensory and behavioral contexts.

Spatial effects of shifting prisms on properties of posterior parietal cortex neurons.

The posterior parietal cortex contains neurons that respond to visual stimulation and motor behaviour. The objective of the current study was to test short-term adaptation in neurons in macaque area 7a and the dorsal prelunate during visually guided reaching using Fresnel prisms that displaced the visual field. The visual perturbation shifted the eye position and created a mismatch between perceived and actual reach location. Two non-human primates were trained to reach to visual targets before, during and after prism exposure while fixating the reach target in different locations. They were required to reach to the physical location of the reach target and not the perceived, displaced location. While behavioural adaptation to the prisms occurred within a few trials, the majority of neurons responded to the distortion either with substantial changes in spatial eye position tuning or changes in overall firing rate. These changes persisted even after prism removal. The spatial changes were not correlated with the direction of induced prism shift. The transformation of gain fields between conditions was estimated by calculating the translation and rotation in Euler angles. Rotations and translations of the horizontal and vertical spatial components occurred in a systematic manner for the population of neurons suggesting that the posterior parietal cortex retains a constant representation of the visual field remapping between experimental conditions.

Optical imaging of visually guided reaching in macaque posterior parietal cortex.

Sensorimotor transformation for reaching movements in primates requires a large network of visual, parietal, and frontal cortical areas. We performed intrinsic optical imaging over posterior parietal cortex including areas 7a and the dorsal perilunate in macaque monkeys during visually guided hand movements. Reaching was performed while foveating one of nine static reach targets; thus eye-position-varied concurrently with reach position. The hemodynamic reflectance signal was analyzed during specific phases of the task including pre-reach, reach, and touch epochs. The eye position maps changed substantially as the task progressed: First, direction of spatial tuning shifted from a weak preference close to the center to the lower eye positions in both cortical areas. Overall tuning strength was greater in area 7a. Second, strength of spatial tuning increased from the early pre-reach to the later touch epoch. These consistent temporal changes suggest that dynamic properties of the reflectance signal were modulated by task parameters. The peak amplitude and peak delay of the reflectance signal showed considerable differences between eye position but were similar between areas. Compared with a detection task using a lever response, the reach task yielded higher amplitudes and longer delays. These findings demonstrate a spatially tuned topographical representation for reaching in both areas and suggest a strong synergistic combination of various feedback signals that result in a spatially tuned amplification of the hemodynamic response in posterior parietal cortex.

Two-photon scanning microscopy of in vivo sensory responses of cortical neurons genetically encoded with a fluorescent voltage sensor in rat.

A fluorescent voltage sensor protein "Flare" was created from a Kv1.4 potassium channel with YFP situated to report voltage-induced conformational changes in vivo. The RNA virus Sindbis introduced Flare into neurons in the binocular region of visual cortex in rat. Injection sites were selected based on intrinsic optical imaging. Expression of Flare occurred in the cell bodies and dendritic processes. Neurons imaged in vivo using two-photon scanning microscopy typically revealed the soma best, discernable against the background labeling of the neuropil. Somatic fluorescence changes were correlated with flashed visual stimuli; however, averaging was essential to observe these changes. This study demonstrates that the genetic modification of single neurons to express a fluorescent voltage sensor can be used to assess neuronal activity in vivo.

Two-photon imaging of calcium in virally transfected striate cortical neurons of behaving monkey.

Two-photon scanning microscopy has advanced our understanding of neural signaling in non-mammalian species and mammals. Various developments are needed to perform two-photon scanning microscopy over prolonged periods in non-human primates performing a behavioral task. In striate cortex in two macaque monkeys, cortical neurons were transfected with a genetically encoded fluorescent calcium sensor, memTNXL, using AAV1 as a viral vector. By constructing an extremely rigid and stable apparatus holding both the two-photon scanning microscope and the monkey's head, single neurons were imaged at high magnification for prolonged periods with minimal motion artifacts for up to ten months. Structural images of single neurons were obtained at high magnification. Changes in calcium during visual stimulation were measured as the monkeys performed a fixation task. Overall, functional responses and orientation tuning curves were obtained in 18.8% of the 234 labeled and imaged neurons. This demonstrated that the two-photon scanning microscopy can be successfully obtained in behaving primates.

Neural representation during visually guided reaching in macaque posterior parietal cortex.

Visually guided hand movements in primates require an interconnected network of various cortical areas. Single unit firing rate from area 7a and dorsal prelunate (DP) neurons of macaque posterior parietal cortex (PPC) was recorded during reaching movements to targets at variable locations and under different eye position conditions. In the eye position-varied task, the reach target was always foveated; thus eye position varied with reach target location. In the retinal-varied task, the monkey reached to targets at variable retinotopic locations while eye position was kept constant in the center. Spatial tuning was examined with respect to temporal (task epoch) and contextual (task condition) aspects, and response fields were compared. The analysis showed distinct tuning types. The majority of neurons changed their gain field tuning and retinotopic tuning between different phases of the task. Between the onset of visual stimulation and the preparatory phase (before the go signal), about one half the neurons altered their firing rate significantly. Spatial response fields during preparation and initiation epochs were strongly influenced by the task condition (eye position varied vs. retinal varied), supporting a strong role of eye position during visually guided reaching. DP neurons, classically considered visual, showed reach related modulation similar to 7a neurons. This study shows that both area 7a and DP are modulated during reaching behavior in primates. The various tuning types in both areas suggest distinct populations recruiting different circuits during visually guided reaching.

Functional organization of temporal frequency selectivity in primate visual cortex.

Several studies have shown that neurons with similar response properties are arranged together in domains across primary visual cortex (V1). An orderly pattern of domains has been described for preferences to ocular dominance, orientation, and spatial frequency. Temporal frequency preference, another important attribute of the visual scene, also might be expected to map into different domains. Using optical imaging and a variety of quantitative methods, we examined how temporal frequency selectivity is mapped in V1 of the prosimian primate, bush baby (Otolemur garnetti). We found that unlike other attribute maps, selectivity for different temporal frequencies is arranged uniformly across V1 with no evidence of local clustering. Global tuning for temporal frequency, based on magnitude of response, showed a good match to previous tuning curves for single neurons. A peak response was found around 2.0 Hz, with smaller attenuation at lower temporal frequencies than at higher frequencies. We also examined whether the peak temporal frequency response differed between anatomical compartments defined by cytochrome oxidase (CO). No significant differences in the preference for temporal frequency were found between these CO compartments. Our findings show that key sensory attributes that are linked in perception can be organized in quite distinct ways in V1 of primates.

A functional architecture of optic flow in the inferior parietal lobule of the behaving monkey.

The representation of navigational optic flow across the inferior parietal lobule was assessed using optical imaging of intrinsic signals in behaving monkeys. The exposed cortex, corresponding to the dorsal-most portion of areas 7a and dorsal prelunate (DP), was imaged in two hemispheres of two rhesus monkeys. The monkeys actively attended to changes in motion stimuli while fixating. Radial expansion and contraction, and rotation clockwise and counter-clockwise optic flow stimuli were presented concentric to the fixation point at two angles of gaze to assess the interrelationship between the eye position and optic flow signal. The cortical response depended upon the type of flow and was modulated by eye position. The optic flow selectivity was embedded in a patchy architecture within the gain field architecture. All four optic flow stimuli tested were represented in areas 7a and DP. The location of the patches varied across days. However the spatial periodicity of the patches remained constant across days at approximately 950 and 1100 microm for the two animals examined. These optical recordings agree with previous electrophysiological studies of area 7a, and provide new evidence for flow selectivity in DP and a fine scale description of its cortical topography. That the functional architectures for optic flow can change over time was unexpected. These and earlier results also from inferior parietal lobule support the inclusion of both static and dynamic functional architectures that define association cortical areas and ultimately support complex cognitive function.

Spatiotemporal dynamics of the functional architecture for gain fields in inferior parietal lobule of behaving monkey.

Intrinsic optical imaging has revealed a representation of eye position smoothly mapped across the surface of the inferior parietal lobule in behaving monkeys. We demonstrate here that blood vessels imaged along with the cortex have large signals tuned sometimes, but not always, to match the surrounding tissue. The relationship between the vessels and surrounding tissue in both space and time was explored using independent component analysis (ICA). Working only with single-trial data, ICA discovered a sequence of regions corresponding to the vascular propagation of activated signals from remote loci into the blood vessels. The vascular signals form a novel map of cortical function--the functional angioarchitecture--superimposed upon the cortical functional architecture. Furthermore, the incorporation of temporal aspects in optical data permitted the tuning of the inferior parietal lobule to be tracked in time through the task, demonstrating the expression of unusual tuning properties that might be exploited for higher cognitive functions.

Attentional modulation of receptive field structure in area 7a of the behaving monkey.

Spatial attention modulates the activity of inferior parietal neurons. A statistically rigorous approach to classical retinotopic mapping was used to quantify the receptive fields of area 7a neurons under 2 attentional conditions. Measurements were made with retinal stimulation held constant and the locus of attention manipulated covertly. Both tasks required central fixation but differed in the locus of covert attention (either on the center fixation point or on a peripheral square target in one of 25 locations). The neuron's identity over the recording session was confirmed using chaos theory to characterize unique temporal patterns. Sixty-six percent of the neurons changed prestimulus activity based on task state. Retinotopic mapping showed no evidence for foveal sparing. Attentional factors influenced visual responses for approximately 30% of the neurons. Two types of modulation were equally observed. One group of cells had a multiplicative scaling of response, with equal instances of enhancement and suppression. A second group of cells had a complex interaction of visual and attentional signals, such that spatial tuning was subject to a nonlinear modulation across the visual field based on attentional constraints. These 2 cell groups may have different roles in the shift of attention preceding motor behaviors and may underlie shifts in parietal retinotopic maps observed with intrinsic optical imaging.

Functional architecture of spatial attention in the parietal cortex of the behaving monkey.

Functional architectures facilitate orderly transmittal of representations between cortices, allow for local interactions between neurons, and ensure a uniform distribution of feature representations with respect to larger-scale topographies. We sought to correlate such topographies with internal cognitive states. A psychophysical task for which the monkey was required to detect a change in one of two identical peripheral expanding flow fields tested for spatial shifts of attention. The monkey was cued as to which flow would change with a small cue near the fixation points. Reaction time data indicate that the monkey's performance in the optic flow detection task depended on the location of the cue. Using optical imaging of intrinsic signals, we show that a monkey's internally generated locus of attention is correlated with an 800-860 microm patchy topological architecture across the cortical surface of the inferior parietal lobule. The attentional patches vary in location but are stable in spatial frequency. The patches are embedded in a larger-scale and stable representation of eye position. Trial-by-trial analysis of the images indicates that the organizational scheme with simultaneous stable and variable subcomponents occurs within the experiment of 1 d, as well as across days. This novel functional architecture is the first to be correlated with attentional mechanisms and could support a fine-scale functional architecture underlying hemispatial neglect, an attentional deficit caused by parietal lesions.

Functional architecture of retinotopy in visual association cortex of behaving monkey.

While the receptive field properties of single neurons in the inferior parietal cortex have been quantitatively described from numerous electrical measurements, the visual topography of area 7a and the adjacent dorsal prelunate area (DP) remains unknown. This lacuna may be a technical byproduct of the difficulty of reconstructing tens to hundreds of penetrations, or may be the result of varying functional retinotopic architectures. Intrinsic optical imaging, performed in behaving monkey for extended periods of time, was used to evaluate retinotopy simultaneously at multiple positions across the cortical surface. As electrical recordings through an implanted artificial dura are difficult, the measurement and quantification of retinotopy with long-term recordings was validated by imaging early visual cortex (areas V1 and V2). Retinotopic topography was found in each of the three other areas studied within a single day's experiment. However, the ventral portion of DP (DPv) had a retinotopic topography that varied from day to day, while the more dorsal aspects (DPd) exhibited consistent retinotopy. This suggests that the dorsal prelunate gyrus may consist of more than one visual area. The retinotopy of area 7a also varied from day to day. Possible mechanisms for this variability across days are discussed as well as its impact upon our understanding of the representation of extrapersonal space in the inferior parietal cortex.

Three-dimensional structure-from-motion selectivity in the anterior superior temporal polysensory area, STPa, of the behaving monkey.

Human and non-human primates are able to perceive three-dimensional structure from motion displays. Three-dimensional structure-from-motion (object-motion) displays were used to test the hypothesis that neurons in the anterior division of the superior temporal polysensory area (STPa) of monkeys can selectively respond to three-dimensional structure-from-motion. Monkeys performed a reaction time task that required the detection of a change in the fraction of structure in three-dimensional transparent sphere displays. Neurons were able to distinguish structured and unstructured three-dimensional optic flow. These cells could differentiate the change in structure-from-motion at stimulus presentation and when the animal was detecting the amount of structure in the display. Some of these neurons were also tuned for characteristics of the sphere stimuli. Cells were also tested with navigational motion and many were found to respond both to three-dimensional structure-from-motion and navigational motion. These results suggest that STPa neurons represent specific aspects of three-dimensional surface structure and that neurons within STPa contribute to the perception of three-dimensional structure-from-motion.

Functional architecture of eye position gain fields in visual association cortex of behaving monkey.

In the behaving monkey, inferior parietal lobe cortical neurons combine visual information with eye position signals. However, an organized topographic map of these neurons' properties has never been demonstrated. Intrinsic optical imaging revealed a functional architecture for the effect of eye position on the visual response to radial optic flow. The map was distributed across two subdivisions of the inferior parietal lobule, area 7a and the dorsal prelunate area, DP. Area 7a contains a representation of the lower eye position gain fields while area DP represents the upper eye position gain fields. Horizontal eye position is represented orthogonal to the vertical eye position across the medial lateral extents of the cortices. Similar topographies were found in three hemispheres of two monkeys; the horizontal and vertical gain field representations were not isotropic with a greater modulation found with the vertical. Monte Carlo methods demonstrated the significance of the maps, and they were verified in part using multiunit recordings. The novel topographic organization of this association cortex area provides a substrate for constructing representations of surrounding space for perception and the guidance of motor behaviors.

A decoding problem in dynamics and in number theory.

Given a homeomorphism f of the circle, any splitting of this circle in two semiopen arcs induces a coding process for the orbits of f, which can be determined by recording the successive arcs visited by the orbit. The problem of describing these codes has a two hundred year history (that we briefly recall) in the particular case when the arcs are limited by a point and its image; in modern language, it is the kneading theory of such maps, and as such is relevant for our understanding of dynamical problems involving oscillations. This paper deals with questions attached to the general case, a problem considered by many mathematicians in the 50's and 60's in the case where f is a rotation, and which has recently found some applications in physiology. We show that, except for trivial cases, any code determines the rotation number, up to the orientation, of the homeomorphism which generates it. In the case the code is periodic, we can also determine whether or not it can be generated in this way. An equivalent problem in arithmetic consists of finding +/-p, knowing a collection of classes in Z/qZ of the form {m,m+p,.,m+(k-1)p}, where 2