Laminar Organization of Response Properties in Primary Visual Cortex of the Gray Squirrel(Sciurus carolinensis)

Abstract

. The gray squirrel (Sciurus carolinensis) is a diurnal highly visual rodent with a cone-rich retina. To determine which features of visual cortex are common to highly visual mammals and which are restricted to non-rodent species, we studied the laminar organization of response properties in primary visual area V1 of isoflurane-anesthetized squirrels using extra-cellular single-unit recording and sinusoidal grating stimuli. Of the responsive cells, 75% were tuned for orientation. Only 10% were directionally selective, almost all in layer 6, a layer receiving direct input from the dorsal lateral geniculate nucleus (LGN). Cone opponency was widespread but almost absent from layer 6. Median optimal spatial frequency tuning was 0.21 cycles/°. Median optimal temporal frequency a high 5.3 Hz. Layer 4 had the highest percentage of simple cells and shortest latency (26 ms). Layers 2/3 had the lowest spontaneous activity and highest temporal frequency tuning. Layer 5 had the broadest spatial frequency tuning and most spontaneous activity. At the layer 4/5 border were sustained cells with high cone opponency. Simple cells, determined by modulation to drifting sinusoidal gratings, responded with shorter latencies, were more selective for orientation and direction, and were tuned to lower spatial frequencies. A comparison with other mammals shows that although the laminar organization of orientation selectivity is variable, the cortical input layers contain more linear cells in most mammals. Nocturnal mammals appear to have more orientation-selective neurons in V1 than diurnal mammals of similar size.

Emergence of Orientation Selectivity in the Mammalian Visual Pathway

“…In cat V1, orientation selectivity is organized in a columnar fashion (Hubel and Wiesel, 1963), whereas in mouse V1 no such organization is evident (Ohki et al, 2005). Even in the gray squirrel, a highly visual rodent with strong cortical orientation selectivity, no clear functional organization for orientation selectivity exists in V1 (Heimel et al, 2005). Lagomorphs, similar to rodents, lack an orientation map in visual cortex, although a clustering of orientation preferences in neurons has been reported Murphy and Berman, 1979) (Fig.…”

“…There are many possible combinations of receptive fields that could generate orientation selectivity, including randomly distributed inputs (Hansel and Van Vreeswijk, 2012) or oriented receptive fields spatially aligned to generate a distinct orientation selectivity. The presence of subcortical orientation selectivity strongly suggests feedforward inheritance in generating cortical selectivity, but it is possible for this selectivity to be discarded and regenerated within V1.…”

Weak orientation and direction selectivity in lateral geniculate nucleus representing central vision in the gray squirrelSciurus carolinensis

“…Adult gray squirrels of either sex weighting 475-700 g were prepared for single-unit recording using the methods described in Van Hooser et al (2003) and Heimel et al (2005). In brief, animals were initially anesthetized with a mixture of ketamine and acepromazine maleate (90 mg/ml ketamine, 0.91 mg/ml acepromazine maleate, and 0.5 ml/kg initial dose im).…”

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

“…After tracer injections, the skin was sutured and the animal recovered on a heated blanket. For physiology, we used an anesthetized preparation that has been described previously (Van Hooser et al, 2003;Heimel et al, 2005). Squirrels were initially anesthetized with a mixture of ketamine and acepromazine maleate, maintained with isoflurane, and paralyzed with gallamine triethiodide.…”