V1 connections reveal a series of elongated higher visual areas in the California ground squirrel, Otospermophilus beecheyi

Abstract

For studies of visual cortex organization, mouse is becoming an increasingly more often used model. In addition to its genetic tractability, the relatively small area of cortical surface devoted to visual processing simplifies efforts in relating the structure of visual cortex to visual function. However, the nature of this compact organization can make some comparisons to the much larger non-human primate visual cortex difficult. The squirrel, as a highly visual rodent offers a useful means for better understanding how mouse and monkey cortical organization compares. More in line with primates than their nocturnal rodent cousin, squirrels rely much more on sight and have evolved a larger expanse of cortex devoted to visual processing. To reveal the detailed organization of visual cortex in squirrels, we injected a highly sensitive monosynaptic retrograde tracer (glycoprotein deleted rabies virus) into several locations of primary visual cortex (V1) in California ground squirrels. The resulting pattern of connectivity revealed an organizational scheme in the squirrel that retains some of the basic features of the mouse visual cortex along the medial and posterior borders of V1, but unlike mouse has an elaborate and extensive pattern laterally that is more similar to the early visual cortex organization found in monkeys. In this way, we show that the squirrel can serve as a useful model for comparison to both mouse and primate visual systems, and may help facilitate comparisons between these two very different yet widely used animal models of visual processing.

Cortical projections to the superior colliculus in grey squirrels (Sciurus carolinensis)

“…Additionally, when injections within the superior colliculus were separate and non‐overlapping, the patches of cortical label were also non‐overlapping, providing evidence for visuotopically organized fields. Recent studies in ground squirrel have suggested that multiple topographically organized cortical fields are represented between area 18 and TP (Negwer et al ., ). It is likely that the patchy pattern of SC projecting cells within OTc in our current study reflects a similar organization scheme in the grey squirrel.…”

“…For instance, early reports have combined OTc and OTr into a single area, area 19 (Hall et al ., ; Kaas et al ., ; Wong & Kaas, ); while others have included the presence of a middle lateral (ML) and lateral (L) areas between an area V3 and TP (Paolini & Sereno, ). A recent study in California ground squirrels has suggested another pattern of cortical organization (Negwer et al ., ), which includes ML and L, but includes additional areas separating these structures form V1. This organization scheme a long cortical area, V3, which runs along the central majority of V2 with an area V3a, and P located along the most rostromedial or caudolateral portions of V2, respectively.…”

“…Similar but somewhat different depictions of visual cortex organization in ground squirrels have been presented by Paolini & Sereno () and Negwer et al . (). In this study, we used the organization scheme of Wong & Kaas, (see Fig.…”

“…Squirrels are of special interest as a highly visual rodent with a well‐laminated superior colliculus that is roughly 10 times larger than expected for a rat of similar size (Le Gros Clark, ; Lane et al ., ; Kaas & Collins, ). In addition, temporal cortex is greatly expanded in squirrels, and much of the cortex located between V1 and primary somatosensory cortex has visual functions (Kaas et al ., , ; Paolini & Sereno, ; Van Hooser & Nelson, ; Wong & Kaas, ; Wong et al ., ; Negwer et al ., ). Other cortical areas, such as somatosensory areas and areas of frontal cortex may also project to the superior colliculus (Aronoff et al ., Wise & Jones, ; Harvey & Worthington, ; Hoffer et al ., ; Comoli et al ., ; Rhoades, ; Collins et al ., ; Baldwin et al ., ; Baldwin et al ., ; Cerkevich et al ., ).…”

Cell type specific tracing of the subcortical input to primary visual cortex from the basal forebrain

“…Visual perception occurs through a complex network of cortical processing that relies on driving, modulating, and integrating interconnectivity with subcortical visual structures as studied extensively in rodents (Guillery & Sherman, ; Krubitzer, Campi, & Cooke, ; Marshel, Garrett, Nauhaus, & Callaway, ; Niell, ; Negwer, Liu, Schubert, & Lyon, ; Seabrook, Burbridge, Crair, & Huberman, ), carnivores (Reid & Alonso, ; Liu, Hashemi‐Nezhad, & Lyon, ; Hashemi‐Nezhad & Lyon, ) nonhuman primates (Felleman & Van Essen, ; Casagrande, ; Lyon et al, ; Casagrande, Sáry, Royal, & Ruiz, ; Kaas, ), and close relatives such as the tree shrew (Casagrande & Harting, ; Lyon, Jain, & Kaas, ; Casagrande, Xu, & Sáry, ). The lateral geniculate nucleus, the superior colliculus and the pulvinar nucleus, are among the most studied subcortical visual regions, having been subject to decades of anatomical and functional investigation by Vivien Casagrande and her colleagues in tree shrew (i.e., Casagrande, Harting, Hall, Diamond, & Martin, ; Lyon, Jain, & Kaas, , b; Vanni, Thomas, Petry, Bickford, & Casanova, ) and primate (i.e., Fitzpatrick, Carey, & Diamond, ; Lachica & Casagrande, ; Stepniewska & Kaas, ; Xu et al, ; Nassi, Lyon, & Callaway, ; Imura & Rockland, ; Kaas & Lyon, ; Lyon, Nassi, & Callaway, ; Purushothaman, Marion, Li, & Casagrande, ; Cerkevich, Lyon, Balaram, & Kaas, ), and by many others in rodent (i.e., Lysakowski, Standage, & Benevento, ; Sanderson, Dreher, & Gayer, ; Van Hooser & Nelson, ; Marshel, Kaye, Nauhaus, & Callaway, ; Cruz‐Martín et al, ; Tohmi, Meguro, Tsukano, Hishida, & Shibuki, ; Roth et al, ; Seabrook et al, ; Zhou, Maire, Masterson, & Bickford, ; Zhou, Masterson, Damron, Guido, & Bickford, ).…”