Orientation Selectivity without Orientation Maps in Visual Cortex of a Highly Visual Mammal

Abstract

In mammalian neocortex, the orderly arrangement of columns of neurons is thought to be a fundamental organizing principle. In primary visual cortex (V1), neurons respond preferentially to bars of a particular orientation, and, in many mammals, these orientationselective cells are arranged in a semiregular, smoothly varying map across the cortical surface. Curiously, orientation maps have not been found in rodents or lagomorphs. To explore whether this lack of organization in previously studied rodents could be attributable to low visual acuity, poorly differentiated visual brain areas, or small absolute V1 size, we examined V1 organization of a larger, highly visual rodent, the gray squirrel. Using intrinsic signal optical imaging and single-cell recordings, we found no evidence of an orientation map, suggesting that formation of orientation maps depends on mechanisms not found in rodents. We did find robust orientation tuning of single cells, and this tuning was invariant to stimulus contrast. Therefore, it seems unlikely that orientation maps are important for orientation tuning or its contrast invariance in V1. In vertical electrode penetrations, we found little evidence for columnar organization of orientation-selective neurons and little evidence for local anisotropy of orientation preferences. We conclude that an orderly and columnar arrangement of functional response properties is not a universal characteristic of cortical architecture.

Dominant Vertical Orientation Processing without Clustered Maps: Early Visual Brain Dynamics Imaged with Voltage-Sensitive Dye in the Pigeon Visual Wulst

“…The functions and origins underlying the orderly clustering of like-preferring orientation-selective V1 neurons is again under intense debate after the discovery that these cells are not clustered in the squirrel V1 (Van Hooser et al, 2005). Furthering the discussion, orientation pinwheels analogous to those found in cat and monkey V1 have been found in the barn owl visual Wulst (Liu and Pettigrew, 2003).…”

“…Against the owl, the pigeon Wulst may be less well differentiated in cytoarchitecture (Karten et al, 1973), receives less afferent input from the GLd, and has neurons with larger receptive fields [4.5° (Miceli et al, 1979) vs 1-2°in owls (Pettigrew, 1979)]. However, although lesser visual system differentiation could be one of the factors explaining the lack of maps in the pigeon, studies in mammals argue against a clear role of advanced visual system development in the establishment of orientation maps (Van Hooser et al, 2005).…”

“…In birds, the maximal overlap is 40 -50°(kestrels) versus 140 -150°(primates) in mammals. a Orientation maps: human (Yacoub et al, 2008); macaque (Blasdel and Salama, 1986); owl monkey (Xu et al, 2004); marmoset (McLoughlin and Schiessl, 2006); cat (Bonhoeffer and Grinvald, 1991); ferret (Weliky and Katz, 1994); tree shrew (Bosking et al, 1997); squirrel (Van Hooser et al, 2005); rat (Ohki et al, 2005); mouse, electrophysiology (Dräger, 1975); rabbit, electrophysiology (Bousfield, 1977;Murphy and Berman, 1979); barn owl (Liu and Pettigrew, 2003). b Binocular overlap and orbit convergence.…”

“…The references for these values were mainly derived from the study by Heesy (2004), his Table 1. Human (Vakkur and Bishop, 1963); macaque (Vakkur and Bishop, 1963;Ross, 1995); owl monkey (Allman and McGuinness, 1988); marmoset (Cartmill, 1971;Fritsches and Rosa, 1996); cat (Hughes, 1976;Arrese et al, 1999;Finarelli and Goswami, 2009); ferret (Garipis and Hoffmann, 2003); tree shrew (Hughes, 1977); squirrel (Kaas et al, 1972;Van Hooser et al, 2005); rat (Arrese et al, 1999); mouse (Dräger, 1978;Arrese et al, 1999); rabbit (Wall, 1942;Hughes and Vaney, 1982); barn owl (Iwaniuk et al, 2008); pigeon (Iwaniuk et al, 2008). more prominent at lower speeds because of the specific spatiotemporal bandwidth of visual neurons.…”

Lack of Patchy Horizontal Connectivity in Primary Visual Cortex of a Mammal without Orientation Maps

“…Although individual cells show orientation selectivity with tuning widths similar to other mammals, there is no map of orientation selectivity, and adjacent neurons often show different orientation preferences (Tiao and Blakemore, 1976;Metín et al, 1988;Ohki et al, 2005;Van Hooser et al, 2005). The absence of orientation maps in rodents raises questions about fundamental principles of horizontal connectivity in cortex and its influence on functional properties.…”