Spatial clustering of orientation preference in primary visual cortex of the large rodent agouti

Abstract

Summary All rodents investigated so far possess orientation-selective neurons in the primary visual cortex (V1) but – in contrast to carnivores and primates – no evidence of periodic maps with pinwheel-like structures. Theoretical studies debating whether phylogeny or universal principles determine development of pinwheels point to V1 size as a critical constraint. Thus, we set out to study maps of agouti, a big diurnal rodent with a V1 size comparable to cats'. In electrophysiology, we detected interspersed orientation and direction-selective neurons with a bias for horizontal contours, corroborated by homogeneous activation in optical imaging. Compatible with spatial clustering at short distance, nearby neurons tended to exhibit similar orientation preference. Our results argue against V1 size as a key parameter in determining the presence of periodic orientation maps. They are consistent with a phylogenetic influence on the map layout and development, potentially reflecting distinct retinal traits or interspecies differences in cortical circuitry.

Editorial: Cortical Maps: Data and Models

“…Although phylogeny is currently the best predictor, an alternative, more directly related to visual system function, is the ratio of central and peripheral ganglion cell densities. This idea is consistent with existing data as well as more recent findings that the agouti (a large rodent) lacks maps (Ferreiro et al, 2021) and that wallabies have them (Jung, 2020).…”

The Organization of Somatostatin-Immunoreactive Cells in the Visual Cortex of the Gerbil

“…Recently, the orientation- and direction-selective neurons and their spatial layout have been characterized in the primary VC of the large diurnal rodent agoutis. Neurons exhibited orientation and direction preferences in agoutis, with a bias for horizontal contours [ 124 ]. The aggregate classical receptive field of agoutis was similar to that of cat areas 17 and 18 and was smaller than that of nocturnal rats and mice [ 124 ].…”

“…Neurons exhibited orientation and direction preferences in agoutis, with a bias for horizontal contours [ 124 ]. The aggregate classical receptive field of agoutis was similar to that of cat areas 17 and 18 and was smaller than that of nocturnal rats and mice [ 124 ]. However, the response properties, such as orientation and direction selectivity, simple and complex cells, and spatial and temporal tuning, that have been fairly well-documented in diurnal squirrels, have not yet been well-studied in gerbils.…”

“…However, the response properties, such as orientation and direction selectivity, simple and complex cells, and spatial and temporal tuning, that have been fairly well-documented in diurnal squirrels, have not yet been well-studied in gerbils. Future studies should elucidate these response properties in gerbils to better understand the diurnal gerbil visual system and the diverse functional organization of the rodent VC as cortical functional architecture can vary greatly from species to species [ 118 , 123 , 124 ].…”

Orientation pinwheels in primary visual cortex of a highly visual marsupial

“…Rodents and rabbits, which are also eutherian mammals, have the same retinotopic representation, but orientation-selective neurons within a given visual field location are distributed in a nonperiodic fashion, generating salt-and-pepper orientation preference (OP) maps (11,12). Some studies (13)(14)(15) report spatial clustering at very short distances in mouse and agouti, where neighboring neurons exhibit similar OPs, but the neurons are not organized into pinwheel orientation maps. This is the case even in the squirrel (12), which is a highly visual rodent with a V1 similar in all obvious respects to that of the eutherian ferret, which has a pinwheel orientation map (5).…”