A micro-architecture for binocular disparity and ocular dominance in visual cortex

Abstract

In invertebrate predators like the praying mantis and vertebrate predators such as wild cats, the ability to detect small differences in inter-ocular retinal disparities is a critical means for accurately determining the depth of moving objects such as prey1. In mammals, the first neurons along the visual pathway that encode binocular disparities are found in the visual cortex. However, a precise functional architecture for binocular disparity has never been demonstrated in any species, and coarse maps for disparity have been found in only one primate species2,3. Moreover, the dominant approach for assaying the developmental plasticity of binocular cortical neurons employed monocular tests of ocular dominance to infer binocular function4. The few studies that examined the relationship between ocular dominance and binocular disparity of individual cells used single-unit recordings and have provided conflicting results as to whether ocular dominance can predict the selectivity or sensitivity to binocular disparity5–9. Here we use two-photon calcium imaging to sample the response to monocular and binocular visual stimuli from nearly every adjacent neuron in a small region of the cat visual cortex, area 18. We show that local circuits for ocular dominance always have smooth and graded transitions from one apparently monocular functional domain to an adjacent binocular region. Most unexpectedly, we discovered a new map in the cat visual cortex that had a precise functional micro-architecture for binocular disparity selectivity. At the level of single cells, ocular dominance was unrelated to binocular disparity selectivity or sensitivity. When the local maps for ocular dominance and binocular disparity both had measurable gradients at a given cortical site, the two gradient directions were orthogonal to each other. Together, these results suggest that from the perspective of the spiking activity of individual neurons, ocular dominance cannot predict binocular disparity tuning. However, the precise local arrangement of ocular dominance and binocular disparity maps provide new clues on how monocular and binocular depth cues may be combined and decoded.

Binocular Disparity Selectivity Weakened after Monocular Deprivation in Mouse V1

“…Fluorescence fluctuations from cells in mouse V1 were strongly modulated by binocular disparities, compared with stimulation of either eye alone or the blank (mean luminance) period, similarly to previous reports of spiking activity (Scholl et al, 2013a) and twophoton calcium imaging in cat (Kara and Boyd, 2009) and mouse V1 (Scholl et al, 2015). In an example neuron ( Fig.…”

“…Experience-dependent plasticity during the developmental critical period (CP) shapes cortical circuit anatomy and functions (Katz and Crowley, 2002;Espinosa and Stryker, 2012). A prime example of CP plasticity is ocular dominance (OD) plasticity, where the OD of V1 neurons shifts toward the open eye following monocular deprivation (MD).…”

Periodic Organization of a Major Subtype of Pyramidal Neurons in Neocortical Layer V

“…Such organization is found in multiple cortical areas including the visual Wiesel, 1974, 1977;Ohki et al, 2006;Kara and Boyd, 2009), somatosensory (Bruno et al, 2003;Andermann and Moore, 2006), motor (Amirikian and Georgopoulos, 2003;Georgopoulos et al, 2007;Dombeck et al, 2009;Komiyama et al, 2010), and frontal cortex (Opris et al, 2011). Our results suggest that cortical functions performed within tens of micrometers in the tangential orientation may be processed by local circuits with a periodic neuronal distribution.…”

“…For example, functional clustering at this scale is observed in the visual and motor cortex Wiesel, 1974, 1977;Ohki et al, 2006;Georgopoulos et al, 2007;Dombeck et al, 2009;Kara and Boyd, 2009). In rodent neocortical layer II/III, the probability of connection between pyramidal neurons located within tens of micrometers in the tangential orientation is higher than that between those located further apart (Holmgren et al, 2003).…”

Grid cells and cortical representation

“…Because orientation is circular, a pinwheel-like arrangement may be required for optimal continuity. Other parameters such as ocular dominance, disparity, spatial frequency, and, of course, position in space are mapped continuously across the entire cortical surface [64][65][66][67][68][69][70] . A notable exception is the saltand-pepper-like organization of the rodent visual cortex [43][44][45] .…”