Functional Specializations of the Ventral Intraparietal Area for Multisensory Heading Discrimination

Chen, Aihua; DeAngelis, Gregory C.; Angelaki, Dora E.

doi:10.1523/jneurosci.4522-12.2013

Cited by 124 publications

(194 citation statements)

References 61 publications

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“…Consistent with previous reports (10,15,28), r noise was positively correlated with r signal in both intact and lesioned animals (ANCOVA; intact, P < 0.001; lesioned, P = 0.03; Fig. 5C).…”

Section: Resultssupporting

confidence: 92%

“…Traditional tools for assessing functional links between single neurons and perceptual decisions include quantification of trial-by-trial correlations between neuronal activity and perceptual reports for ambiguous stimuli (1). Such "choice probabilities" (CPs) have been reported in visual (2-9), parietal (10), and somatosensory (11) cortical areas. Computational studies have also shown that the extent of correlated noise in a pool of neurons profoundly affects CPs (12)(13)(14).…”

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confidence: 99%

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Reduced choice-related activity and correlated noise accompany perceptual deficits following unilateral vestibular lesion

Liu

Dickman

Newlands³

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

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Signals from the bilateral vestibular labyrinths work in tandem to generate robust estimates of our motion and orientation in the world. The relative contributions of each labyrinth to behavior, as well as how the brain recovers after unilateral peripheral damage, have been characterized for motor reflexes, but never for perceptual functions. Here we measure perceptual deficits in a heading discrimination task following surgical ablation of the neurosensory epithelium in one labyrinth. We found large increases in heading discrimination thresholds and large perceptual biases at 1 wk postlesion. Repeated testing thereafter improved heading perception, but vestibular discrimination thresholds remained elevated 3 mo postlesion. Electrophysiological recordings from the contralateral vestibular and cerebellar nuclei revealed elevated neuronal discrimination thresholds, elevated neurometric-to-psychometric threshold ratios, and reduced trial-by-trial correlations with perceptual decisions ["choice probabilities" (CPs)]. The relationship between CP and neuronal threshold was shallower, but not significantly altered, suggesting that smaller CPs in lesioned animals could be largely attributable to greater neuronal thresholds. Simultaneous recordings from pairs of neurons revealed that correlated noise among neurons was also reduced following the lesion. Simulations of a simple pooling model, which takes into account the observed changes in tuning slope and correlated noise, qualitatively accounts for the elevated psychophysical thresholds and neurometric-to-psychometric ratios, as well as the decreased CPs. Thus, cross-labyrinthine interactions appear to play important roles in enhancing neuronal and perceptual sensitivity, strengthening interneuronal correlations, and facilitating correlations between neural activity and perceptual decisions.noise correlation | self-motion | decoding T he search for the neural basis of perception has fascinated neuroscientists for a long time. Traditional tools for assessing functional links between single neurons and perceptual decisions include quantification of trial-by-trial correlations between neuronal activity and perceptual reports for ambiguous stimuli (1). Such "choice probabilities" (CPs) have been reported in visual (2-9), parietal (10), and somatosensory (11) cortical areas. Computational studies have also shown that the extent of correlated noise in a pool of neurons profoundly affects . Until recently, these properties were largely considered the province of cerebral cortex.To better understand how peripheral sensory signals are processed centrally to generate perceptual decisions, Liu et al. (15) used a vestibular heading discrimination task to explore the relationships between neuronal sensitivity, CPs, and correlated noise in vestibular nucleus (VN) and cerebellar nucleus (CN) neurons. These areas receive afferent signals from the vestibular periphery and are interconnected with the thalamo-cortical system (16, 17), the midline vestibulocerebellum (18), the spinal cord ...

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“…Consistent with previous reports (10,15,28), r noise was positively correlated with r signal in both intact and lesioned animals (ANCOVA; intact, P < 0.001; lesioned, P = 0.03; Fig. 5C).…”

Section: Resultssupporting

confidence: 92%

mentioning

confidence: 99%

Reduced choice-related activity and correlated noise accompany perceptual deficits following unilateral vestibular lesion

Liu

Dickman

Newlands³

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

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“…We recorded from area VIP, because VIP neurons exhibit heading tuning based on optic flow (20)(21)(22)(23)(24) that is tolerant to real or visually simulated eye rotations (11,12), and also because VIP neurons respond to smooth pursuit eye movements (25). In addition, previous studies have reported gain fields-changes in the amplitude of heading tuning curves caused by rotations (11,12).…”

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confidence: 99%

Joint representation of translational and rotational components of optic flow in parietal cortex

Sunkara

DeAngelis

Angelaki

2016

Proc. Natl. Acad. Sci. U.S.A.

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Terrestrial navigation naturally involves translations within the horizontal plane and eye rotations about a vertical (yaw) axis to track and fixate targets of interest. Neurons in the macaque ventral intraparietal (VIP) area are known to represent heading (the direction of selftranslation) from optic flow in a manner that is tolerant to rotational visual cues generated during pursuit eye movements. Previous studies have also reported that eye rotations modulate the response gain of heading tuning curves in VIP neurons. We tested the hypothesis that VIP neurons simultaneously represent both heading and horizontal (yaw) eye rotation velocity by measuring heading tuning curves for a range of rotational velocities of either real or simulated eye movements. Three findings support the hypothesis of a joint representation. First, we show that rotation velocity selectivity based on gain modulations of visual heading tuning is similar to that measured during pure rotations. Second, gain modulations of heading tuning are similar for self-generated eye rotations and visually simulated rotations, indicating that the representation of rotation velocity in VIP is multimodal, driven by both visual and extraretinal signals. Third, we show that roughly one-half of VIP neurons jointly represent heading and rotation velocity in a multiplicatively separable manner. These results provide the first evidence, to our knowledge, for a joint representation of translation direction and rotation velocity in parietal cortex and show that rotation velocity can be represented based on visual cues, even in the absence of efference copy signals.self-motion | optic flow | rotation | heading | ventral intraparietal area A s we navigate through the world, our motion can be described as combinations of translations (T) and rotations (R). Patterns of image motion associated with T and R are added together in the retinal flow field during navigation (Fig. 1A). The rotational component of self-motion can arise from a variety of sources, including eye, head, and body rotations as well as traveling along a curved path. Hence, to perform specific tasks, we may need to estimate our translation, rotation, or both. One way that this could be accomplished is by decomposing optic flow into its translational and rotational components (1-6).Information about rotational velocity is necessary for navigational tasks, such as interpreting optic flow to deduce the instantaneous direction of translation in the presence of eye (or head/ body) rotations, estimating the velocity of a tracked object, and determining the curvature of one's trajectory. Despite the importance of representing rotation velocity during self-motion, many psychophysical and electrophysiological studies have mainly considered rotations as something to be "subtracted out" to estimate our direction of translation (5,(7)(8)(9)(10)(11)(12). These studies have shown that the visual system can represent translations with tolerance to rotation but do not address the question of representing rotation in...

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“…Hence, the quest to untangle and exploit the normative rules and principles of multisensory processing will be vital for understanding decision-making in the intersection of sensation, action, and experience. Gu et al 2008) and (B) VIP (from Chen et al 2013a). Data are shown as scatter plots of the ratio of the threshold measured in the combined condition relative to the prediction for optimal cue integration (Eq.…”

Section: Resultsmentioning

confidence: 99%

“…0˚heading denotes straight forward translation, whereas positive/negative numbers indicate rightward/leftward directions, respectively. Data (from Gu et al 2008 andChen et al 2013a) illustrate firing rate means and SE. The numbers on each panel illustrate the "Congruency Index" for each cell.…”

Section: Neural Correlates Of Multisensory Heading Perceptionmentioning

confidence: 99%

How Optic Flow and Inertial Cues Improve Motion Perception

Angelaki

2014

Cold Spring Harb Symp Quant Biol

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Estimating our egocentric heading direction is an important component of navigation. Recent studies have explored how inertial cues from the vestibular system and optic flow signals from the visual system interact to improve perceptual precision and accuracy. Heading precision is improved through multisensory integration, whereas heading accuracy is maintained through multisensory calibration mechanisms. Neural correlates of these behaviors are found in a large interconnected cortical network, although the specific contributions of each area remain to be explored. Whether and how this multisensory selfmotion cortical circuit contributes to navigation and how egocentric heading signals interact with the allocentric representations for foraging and exploration also remain challenges for the future.

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Functional Specializations of the Ventral Intraparietal Area for Multisensory Heading Discrimination

Cited by 124 publications

References 61 publications

Reduced choice-related activity and correlated noise accompany perceptual deficits following unilateral vestibular lesion

Reduced choice-related activity and correlated noise accompany perceptual deficits following unilateral vestibular lesion

Joint representation of translational and rotational components of optic flow in parietal cortex

How Optic Flow and Inertial Cues Improve Motion Perception

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