The links between neural activity, perception and cognition are poorly understood. This proposal advances color as a model system to fill these gaps in knowledge. Color is an essential feature of visual experience, and much is known about how cone signals from the eye are encoded and transmitted to the cortex. But surprisingly little is known about the mechanisms that decode these signals to bring about perceived colors and guide perceptual decisions. Two competing decoding schemes have been proposed: an interval code, which requires a population of cells with sharp chromatic tuning that together encompass all color space, coupled with a winner- take-all rule; and a population code, which needs at minimum two groups of color-tuned neurons, coupled with a weighted-average rule. It is unclear which groups of neurons within the cerebral cortex are involved. One hint comes from lesions of inferior temporal cortex (IT) in rhesus monkeys, which cause profound color blindness similar to the achromatopsia that accompanies certain cerebral strokes in humans. IT is an expansive region of tissue implicated in many aspects of object coding, and the functional organization of IT is poorly understood. Without this information, it is almost impossible to know which neurons are the most likely to be contributing to color processing. Possible organizational schemes include a modular model comprising uniquely specialized areas; a distributed-processing model; or a hybrid model, consisting of a series of hierarchical stages, each comprising a full complement of functional subregions.
Aim 1 calls for a battery of functional magnetic resonance imaging (fMRI) experiments in alert monkey that will determine the distribution of color-coding regions in IT, their functional connectivity and relationship to other functionally defined regions to test which model accounts for the organization of IT.
Aim 2 outlines fMRI-guided microelectrode recordings of IT color regions paired with microstimulation while monkeys perform color tasks, to test the causal link between neural activity and perceived color, and to determine which of the two decoding schemes, interval or population, is implemented in IT. The research will uncover principles by which perception and cognition emerge from the activity of neural circuits. This information is required to understand the etiology, diagnosis, and treatment of mental illnesses and strokes that impair cognition and perception. Moreover, the work will establish the relationship of higher-order areas between humans and monkeys, which is necessary in order to use monkeys as models of human vision and disease.

Public Health Relevance

The proposed research will provide knowledge of the link between neural activity and visual perception in normal brains, using fMRI-guided microelectrode recording of inferior temporal cortex, an underexplored yet critically important brain region for vision. Understanding these mechanisms is not only important for developing new treatment strategies for mental illnesses and neurological disease, but also for guiding treatments for visual impairment that bypass the eye and exploit those cortical computations that survive the primary insult in blindness. The results will also further knowledge of the biological basis for fMRI, which, despite its widespread use in hospitals and research, is still poorly understood.

Agency
National Institute of Health (NIH)
Institute
National Eye Institute (NEI)
Type
Research Project (R01)
Project #
5R01EY023322-04
Application #
8929251
Study Section
Special Emphasis Panel (ZRG1-IFCN-Q (02))
Program Officer
Araj, Houmam H
Project Start
2013-09-01
Project End
2018-07-31
Budget Start
2015-08-01
Budget End
2016-07-31
Support Year
4
Fiscal Year
2015
Total Cost
$382,200
Indirect Cost
$137,200
Name
Massachusetts Institute of Technology
Department
Type
DUNS #
001425594
City
Cambridge
State
MA
Country
United States
Zip Code
02139
Lafer-Sousa, Rosa; Conway, Bevil R (2017) #TheDress: Categorical perception of an ambiguous color image. J Vis 17:25
Gibson, Edward; Futrell, Richard; Jara-Ettinger, Julian et al. (2017) Color naming across languages reflects color use. Proc Natl Acad Sci U S A 114:10785-10790
Lafer-Sousa, Rosa; Conway, Bevil R; Kanwisher, Nancy G (2016) Color-Biased Regions of the Ventral Visual Pathway Lie between Face- and Place-Selective Regions in Humans, as in Macaques. J Neurosci 36:1682-97
Lafer-Sousa, Rosa; Hermann, Katherine L; Conway, Bevil R (2015) Striking individual differences in color perception uncovered by 'the dress' photograph. Curr Biol 25:R545-6
Hubel, David H; Wiesel, Torsten N; Yeagle, Erin M et al. (2015) Binocular stereoscopy in visual areas V-2, V-3, and V-3A of the macaque monkey. Cereb Cortex 25:959-71
Verhoef, Bram-Ernst; Bohon, Kaitlin S; Conway, Bevil R (2015) Functional architecture for disparity in macaque inferior temporal cortex and its relationship to the architecture for faces, color, scenes, and visual field. J Neurosci 35:6952-68
Gagin, Galina; Bohon, Kaitlin S; Butensky, Adam et al. (2014) Color-detection thresholds in rhesus macaque monkeys and humans. J Vis 14:12
Conway, Bevil R (2014) Color signals through dorsal and ventral visual pathways. Vis Neurosci 31:197-209
Zaidi, Qasim; Marshall, Justin; Thoen, Hanne et al. (2014) Evolution of neural computations: Mantis shrimp and human color decoding. Iperception 5:492-6
Lafer-Sousa, Rosa; Conway, Bevil R (2013) Parallel, multi-stage processing of colors, faces and shapes in macaque inferior temporal cortex. Nat Neurosci 16:1870-8

Showing the most recent 10 out of 11 publications