A major challenge in neuroscience is to understand how neural circuits in the visual cortex compute the response properties of cortical neurons, and how these contribute to visual perception. To study cortical computations, we first need to identify the circuits themselves, and to understand how they are organized with respect to the functional architecture of the visual cortex. The output pathways from the primary visual cortex (V1) to the secondary visual area (V2) are a good model to study cortical computations, because they show a highly specialized organization. It was first thought that three parallel processing pathways to V2 (for the processing of color, form and stereopsis, respectively) leave V1, and segregate into distinct V2 subregions (thick, thin and pale cytochrome-oxidase -CO- stripes). Recent studies have revised this model and proposed that only two pathways to V2 leave V1, one to the thin stripes, the other to both pale and thick stripes. With pale and thick stripes receiving a common message from V1, models of parallel processing in the visual system are being challenged. However, thick and pale stripes segregate their outputs to cortical areas having different functional specialization. This observation, and a critical evaluation of the recent anatomical data, suggests that the pale and thick stripes instead may receive segregated inputs from V1. We propose to use retrograde tracer injections targeted to functionally identified (using optical imaging - OI) specific V2 stripes, and quantitative anatomical methods, to test the hypothesis that more than just two segregated pathways to V2 leave from V1. Using a novel retrograde viral tracer (a genetically modified GFP- expressing rabies virus) to label dendritic and axonal arbors of single V1 output cells, we further propose to examine, at the single cell level, the degree of specialization of the V1 output pathways to different V2 stripes. In particular, we will test the hypothesis that V1 projections to different V2 stripes arise from distinct cell populations. Information on how V1 output pathways are organized with respect to the cortical maps of visual stimulus features in V1 and V2 is necessary to understand their computational role. The response properties of V2 neurons in different CO stripes suggest that thin strips are involved in surface processing, and thick and pale stripes in contour processing. Thick and pale stripes may be further specialized in processing different aspects of object contours. To determine what and how V1 contributes to the response properties of V2 cells, we propose to examine, at the neuronal population and single cell level, how the V1 output pathways to different V2 stripes are organized with respect to the retinotopic maps, and maps of visual stimulus orientation and spatial frequency in V1 and V2. Retrograde tracers and the rabies-GFP virus will be co-injected into specific orientation or spatial frequency domains within specific V2 stripes, identified by OI. The distribution of resulting labeled cells and boutons on the V1 feature maps will be quantitatively analyzed. These studies will provide insight into parallel information processing in the early visual system, and into the kinds of computations that are performed by the V1 output pathways to V2.

Public Health Relevance

Normal vision depends on the orderly development of circuits in the visual cortex and on their intact function. Our studies of the normal circuitry between cortical areas V1 and V2, which are at the early stages of visual processing, will also provide greater insight into the causes and effects of central vision defects when these circuits are damaged by stroke or other insult.

Agency
National Institute of Health (NIH)
Institute
National Eye Institute (NEI)
Type
Research Project (R01)
Project #
5R01EY019743-03
Application #
8106229
Study Section
Central Visual Processing Study Section (CVP)
Program Officer
Steinmetz, Michael A
Project Start
2009-08-01
Project End
2013-07-31
Budget Start
2011-09-30
Budget End
2013-07-31
Support Year
3
Fiscal Year
2011
Total Cost
$357,588
Indirect Cost
Name
University of Utah
Department
Ophthalmology
Type
Schools of Medicine
DUNS #
009095365
City
Salt Lake City
State
UT
Country
United States
Zip Code
84112
Angelucci, Alessandra; Rosa, Marcello G P (2015) Resolving the organization of the third tier visual cortex in primates: a hypothesis-based approach. Vis Neurosci 32:E010
Jeffs, Janelle; Federer, Frederick; Angelucci, Alessandra (2015) Corticocortical connection patterns reveal two distinct visual cortical areas bordering dorsal V2 in marmoset monkey. Vis Neurosci 32:E012
Seyedhosseini, Mojtaba; Shushruth, S; Davis, Tyler et al. (2015) Informative features of local field potential signals in primary visual cortex during natural image stimulation. J Neurophysiol 113:1520-32
Nurminen, Lauri; Angelucci, Alessandra (2014) Multiple components of surround modulation in primary visual cortex: multiple neural circuits with multiple functions? Vision Res 104:47-56
Rosa, Marcello G P; Angelucci, Alessandra; Jeffs, Janelle et al. (2013) The case for a dorsomedial area in the primate 'third-tier' visual cortex. Proc Biol Sci 280:20121372; discussion 20121994
Jeffs, Janelle; Federer, Frederick; Ichida, Jennifer M et al. (2013) High-resolution mapping of anatomical connections in marmoset extrastriate cortex reveals a complete representation of the visual field bordering dorsal V2. Cereb Cortex 23:1126-47
Federer, Frederick; Williams, Delaney; Ichida, Jennifer M et al. (2013) Two projection streams from macaque V1 to the pale cytochrome oxidase stripes of V2. J Neurosci 33:11530-9
Shushruth, S; Nurminen, Lauri; Bijanzadeh, Maryam et al. (2013) Different orientation tuning of near- and far-surround suppression in macaque primary visual cortex mirrors their tuning in human perception. J Neurosci 33:106-19
Shushruth, S; Mangapathy, Pradeep; Ichida, Jennifer M et al. (2012) Strong recurrent networks compute the orientation tuning of surround modulation in the primate primary visual cortex. J Neurosci 32:308-21
Schwabe, Lars; Ichida, Jennifer M; Shushruth, S et al. (2010) Contrast-dependence of surround suppression in Macaque V1: experimental testing of a recurrent network model. Neuroimage 52:777-92

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