This work addresses a question of fundamental significance: how does sensory reafference help maintain perceptual stability during eye and head movements? For example, a rightward eye movement adds leftward motion to the retinal image. This self-produced retinal motion - reafference - must be discounted to compute real-world (e.g., object) motion. Whenever this operation fails, a stationary background seems moving, a phenomenon known as the Filehne illusion. A similar compensation for reafference is necessary when optic flow is used to estimate the direction of self-motion (i.e., heading). Indeed, when tested in the laboratory, subjects are remarkably good at compensating for smooth pursuit eye movements and accuracy is little affected. But where in the brain does this reafference compensation for pursuit take place? Here we propose a 2-pronged approach, where (i) we record simultaneously from the dorsal medial superior temporal area (MSTd), the ventral intraparietal area (VIP), the visual posterior sylvian (VPS) and parieto-occipital area V6 and characterize how visual motion and/or heading tuning changes during pursuit eye and head movements (aim 1), as well as the reference frames in which visual and vestibular heading signals are represented (aim 2);and (ii) we use reversible chemical inactivation to silence neural activity in these areas while monitoring the animals'ability to perform a heading direction discrimination task in the presence of pursuit eye and head movements, as well as the magnitude and direction of the Filehne illusion. Importantly, our experimental design circumvents many technical and interpretational problems in previous studies, whereas optimal decoding analysis will address, not only single neuron, but also population responses. The general principles that we uncover should have wide application to problems in systems neuroscience, ranging from the electric fish to human cognition. In terms of health-related significance, although uncommon, loss of perceptual compensation for reafference has disabling consequences. Recent studies have shown that misattributions of agency in schizophrenia are based on imprecise predictions about the sensory consequences of one's actions;thus, understanding the neural basis of reafference will be important for further investigating this complex cognitive disorder. In addition, this work also addresses the neural basis of self-motion perception and navigation, which is relevant to spatial disorientation deficits in Alzheimer's disease.

Public Health Relevance

The general principles that we uncover should have wide application to problems in systems neuroscience, ranging from the electric fish to human cognition. In terms of health-related significance, although uncommon, loss of perceptual compensation for reafference has disabling consequences. Recent studies have shown that misattributions of agency in schizophrenia are based on imprecise predictions about the sensory consequences of one's actions;thus, understanding the neural basis of reafference will be important for further investigating this complex cognitive disorder. In addition, this work also addresses the neural basis of self-motion perception and navigation, which is relevant to spatial disorientation deficits in Alzheimer's disease.

Agency
National Institute of Health (NIH)
Institute
National Eye Institute (NEI)
Type
Research Project (R01)
Project #
5R01EY017866-09
Application #
8609034
Study Section
Special Emphasis Panel (ZRG1-IFCN-N (02))
Program Officer
Steinmetz, Michael A
Project Start
2007-02-01
Project End
2016-01-31
Budget Start
2014-02-01
Budget End
2015-01-31
Support Year
9
Fiscal Year
2014
Total Cost
$352,125
Indirect Cost
$127,125
Name
Baylor College of Medicine
Department
Neurosciences
Type
Schools of Medicine
DUNS #
051113330
City
Houston
State
TX
Country
United States
Zip Code
77030
Gu, Yong; Angelaki, Dora E; DeAngelis, Gregory C (2014) Contribution of correlated noise and selective decoding to choice probability measurements in extrastriate visual cortex. Elife 3:
Chen, Xiaodong; DeAngelis, Gregory C; Angelaki, Dora E (2014) Eye-centered visual receptive fields in the ventral intraparietal area. J Neurophysiol 112:353-61
Chen, Aihua; Deangelis, Gregory C; Angelaki, Dora E (2013) Functional specializations of the ventral intraparietal area for multisensory heading discrimination. J Neurosci 33:3567-81
Chen, Xiaodong; DeAngelis, Gregory C; Angelaki, Dora E (2013) Eye-centered representation of optic flow tuning in the ventral intraparietal area. J Neurosci 33:18574-82
Chen, Xiaodong; Deangelis, Gregory C; Angelaki, Dora E (2013) Diverse spatial reference frames of vestibular signals in parietal cortex. Neuron 80:1310-21
Chen, Aihua; DeAngelis, Gregory C; Angelaki, Dora E (2011) Convergence of vestibular and visual self-motion signals in an area of the posterior sylvian fissure. J Neurosci 31:11617-27
Liu, Sheng; Dickman, J David; Angelaki, Dora E (2011) Response dynamics and tilt versus translation discrimination in parietoinsular vestibular cortex. Cereb Cortex 21:563-73
Chen, Aihua; DeAngelis, Gregory C; Angelaki, Dora E (2011) A comparison of vestibular spatiotemporal tuning in macaque parietoinsular vestibular cortex, ventral intraparietal area, and medial superior temporal area. J Neurosci 31:3082-94
Chen, Aihua; DeAngelis, Gregory C; Angelaki, Dora E (2011) Representation of vestibular and visual cues to self-motion in ventral intraparietal cortex. J Neurosci 31:12036-52
Gu, Yong; Fetsch, Christopher R; Adeyemo, Babatunde et al. (2010) Decoding of MSTd population activity accounts for variations in the precision of heading perception. Neuron 66:596-609

Showing the most recent 10 out of 24 publications