Orientation selectivity in the visual cortex of the nine-banded armadillo

Abstract

Orientation selectivity in primary visual cortex (V1) has been proposed to reflect a canonical computation performed by the neocortical circuitry. Although orientation selectivity has been reported in all mammals examined to date, the degree of selectivity and the functional organization of selectivity vary across mammalian clades. The differences in degree of orientation selectivity are large, from reports in marsupials that only a small subset of neurons are selective to studies in carnivores, in which it is rare to find a neuron lacking selectivity. Furthermore, the functional organization in cortex varies in that the primate and carnivore V1 is characterized by an organization in which nearby neurons share orientation preference while other mammals such as rodents and lagomorphs either lack or have only extremely weak clustering. To gain insight into the evolutionary emergence of orientation selectivity, we examined the nine-banded armadillo, a species within the early placental clade Xenarthra. Here we use a combination of neuroimaging, histological, and electrophysiological methods to identify the retinofugal pathways, locate V1, and for the first time examine the functional properties of V1 neurons in the armadillo (Dasypus novemcinctus) V1. Individual neurons were strongly sensitive to the orientation and often the direction of drifting gratings. We uncovered a wide range of orientation preferences but found a bias for horizontal gratings. The presence of strong orientation selectivity in armadillos suggests that the circuitry responsible for this computation is common to all placental mammals.NEW & NOTEWORTHY The current study shows that armadillo primary visual cortex (V1) neurons share the signature properties of V1 neurons of primates, carnivorans, and rodents. Furthermore, these neurons exhibit a degree of selectivity for stimulus orientation and motion direction similar to that found in primate V1. Our findings in armadillo visual cortex suggest that the functional properties of V1 neurons emerged early in the mammalian lineage, near the time of the divergence of marsupials.

Keywords: extracellular recording; lateral geniculate nucleus; primary visual cortex.

Fig. 1.

Structural MR and tractographic images of armadillo visual pathways. A: surface rendering of armadillo brain and eyes based on structural MRI data. Cerebellum is to top right, and eyes are to the left. Colored arrows indicate location of coronal sections shown in series. 1–5: rostrocaudal series of structural MR images, showing optic nerve descending from eyes, moving medially and ventrally to optic chiasm. Optic tract then extends caudally and continues dorsally along thalamus to reach LGN. Scale bar is 1 cm. B: reconstructions of optic nerve, tract, and optic radiations in the armadillo. Red and dark blue lines indicate left and right projection from retina, respectively, crossing in the optic chiasm, and continuing to contralateral LGN. Light blue and yellow lines indicate optic radiations from LGN to V1, derived from tractography seeds in the LGN (yellow) or primary visual cortex. Abbreviations used: 3v, third ventricle; A1, primary auditory cortex; a.c., anterior commissure; c.c., corpus callosum; c.n. II, optic nerve; c.n. V, trigeminal nerve; l.g.n., lateral geniculate nucleus; l.v., lateral ventricle; m.g.n., medial geniculate nucleus; nt, nasal turbinates; ob, olfactory bulb; o.c., optic chiasm; olf. t., olfactory tubercle; o.t., optic tract; pit., pituitary gland; S1, primary somatosensory cortex; s.c., superior colliculus; V1, primary visual cortex.

Fig. 2.

Anatomical location and identification of armadillo V1 using myelin and CO staining. A: flattened hemisphere sectioned tangential to cortical surface and stained for myelin. Note dense staining in primary somatosensory and auditory areas, while V1 is moderately stained. R, rostral; M, medial. B: photomicrograph of coronal section through caudal end of armadillo brain stained for cytochrome oxidase histochemistry. Electrode tract (arrowhead) and lesion (*) from recordings in this study are shown. L, lateral; D, dorsal. A1 and V1 are both identified by a densely stained layer IV. Relatively lightly stained region between A1 and V1 was not explored in this study but is expected to correspond to bimodal zone, in which responses to auditory and visual stimuli can be evoked. Scale bar is 1 mm.

Fig. 3.

Retinotopic progression in relation to location in visual cortex. A: receptive field locations for single units recorded along electrode penetrations for case 04-16. The receptive field centers for four neurons are plotted for a single penetration, where the deepest neuron is indicated by the arrowhead. B: as in A, but for two penetrations in case 04-13. The two penetrations are indicated by red and blue symbols. Coordinates used: U, upper; L, lower; C, central; P, periphery. C and D: a sagittal drawing of the armadillo neocortex depicting the electrode trajectory for the two cases. Lines indicate the penetrations along the sagittal plane. Coordinates used: D, dorsal; V, ventral; L, lateral; M, medial. E and F: a dorsal perspective of the armadillo neocortex, where the visual cortex is indicated by the gray shading. The locations of the penetrations are indicated by the arrows. In both cases, penetrations were angled toward the medial bank, as indicated by the arrows. Coordinates used: A, anterior; P, posterior; L, lateral; M, medial.

Fig. 4.

Reconstructed electrode tracks through V1 in case 14-14. A–F: drawings of sections stained for cytochrome oxidase histochemistry, spaced 100 µm apart, ordered rostrocaudally. Electrode tract for one penetration is indicated with number 5 and arrowhead (* in F indicates lesion at end of tract for penetration 5; additional arrowheads indicate other electrode tracts). In all cases, recordings were made through the cortical depths, and lesions were placed to identify the end of the penetration. Here, lv, lateral ventricle; wm, white matter. D–F include representative stained sections. Cortical layer IV was typically densely stained in V1, although in some sections, distinguishing layers III, IV, and V was difficult. G–J: data recording during penetration 5. G shows raster and histograms of the response to orientations for the orientation-selective neuron in H. Two additional neurons recorded in penetration 5 are shown in I and J. Here, spks/s, spikes per second.

Fig. 5.

Orientation and directional selectivity in single units in armadillo V1. A: representative tuning curves from case 14-16 showing weakly tuned (top left) and highly tuned (bottom right) neurons. B: preferred orientation and orientation selectivity indexes for a population of V1 neurons in armadillo V1. Overall, a bias toward horizontal orientations was evident. A range of orientation selectivity was observed, and values were similar to those in rodent V1 [0.385 ± 0.71 (mean ± SD), median = 0.21]. Most neurons in this population were simple cells (F1/F0 > 1). The directional selectivity among neurons was variable but similar to that observed in rodents (0.31 ± 0.26, median = 0.19; DSI, direction selectivity index).

Fig. 6.

Phylogenetic relationships and orientation selectivity in mammalian clades. Increased complexity in functional organization (e.g., columnar organization of orientation selectivity) is observed in V1 of relatively recently derived mammals. Symbols indicate whether there is strong orientation selectivity, whether there is a map of orientation selectivity, and the degree to which the eyes are forward facing. Orientation tuning has not been described in monotremes, but orientation selectivity has been measured in some marsupial species and exists in all placental mammals that have been examined. Data from the current study indicate that strong orientation selectivity is present in Xenarthra, a relatively early-derived placental clade, suggesting that strong orientation tuning may have become prevalent during the placental radiation. Cat, Grinvald et al. (1986) and Hubel and Wiesel (1962); ferret, Chapman et al. (1996); sheep, Clarke et al. (1976); galago, Xu et al. (2005); macaque, Blasdel and Salama (1986); rabbit, Murphy and Berman (1979); mouse, Kondo et al. (2016); hamster, Tiao and Blakemore (1976); Virginia opossum, Christensen and Hill (1970); brushtail possum, Crewther et al. (1984); wallaby, Ibbotson and Mark (2003). *Data obtained solely with electrophysiological recordings.