Figure–ground discrimination in the avian brain: The nucleus rotundus and its inhibitory complex

Abstract

In primates, neurons sensitive to figure-ground status are located in striate cortex (area V1) and extrastriate cortex (area V2). Although much is known about the anatomical structure and connectivity of the avian visual pathway, the functional organization of the avian brain remains largely unexplored. To pinpoint the areas associated with figure-ground segregation in the avian brain, we used a radioactively labeled glucose analog to compare differences in glucose uptake after figure-ground, color, and shape discriminations. We also included a control group that received food on a variable-interval schedule, but was not required to learn a visual discrimination. Although the discrimination task depended on group assignment, the stimulus displays were identical for all three experimental groups, ensuring that all animals were exposed to the same visual input. Our analysis concentrated on the primary thalamic nucleus associated with visual processing, the nucleus rotundus (Rt), and two nuclei providing regulatory feedback, the pretectum (PT) and the nucleus subpretectalis/interstitio-pretecto-subpretectalis complex (SP/IPS). We found that figure-ground discrimination was associated with strong and nonlateralized activity of Rt and SP/IPS, whereas color discrimination produced strong and lateralized activation in Rt alone. Shape discrimination was associated with lower activity of Rt than in the control group. Taken together, our results suggest that figure-ground discrimination is associated with Rt and that SP/IPS may be a main source of inhibitory control. Thus, figure-ground segregation in the avian brain may occur earlier than in the primate brain.

Bilateral lesions of nucleus subpretectalis/interstitio-pretecto-subpretectalis (SP/IPS) selectively impair figure–ground discrimination in pigeons

“…3A illustrates the mean accuracy achieved for each of the three discriminative tasks during first 10 training sessions. Consistent with our earlier results (Acerbo et al, 2012), by the 10th training session, the accuracy in color discrimination, t (8) = 9.11, P < 0.0001, and figure–ground discrimination, t (8) = 3.21, P = 0.01, was statistically above the chance level according to a two-tailed t -test. Shape discrimination accuracy, however, failed to significantly rise above chance, t (8) = 0.60, P = 0.57.…”

“…Consistent with our earlier results (Acerbo et al, 2012 ), by the 10th training session, the accuracy in color discrimination, t (8) = 9.11, P < 0.0001, and fi gure-ground discrimination, t (8) = 3.21, P = 0.01, was statistically above the chance level according to a two-tailed t -test. 3A illustrates the mean accuracy achieved for each of the three discriminative tasks during fi rst 10 training sessions.…”

“…3B), there were no significant correlations of accuracy in color discrimination task with the volume of lesion in either the SP or the IPS (all P ’s ≥ 0.104), suggesting that the lesions of the SP/IPS complex had no discernible effect on color discrimination accuracy. Together with our earlier report (Acerbo et al, 2012), these results strongly imply that the Rt may not be directly involved in color discrimination despite the presence of color-sensitive cells (Wang et al, 1993). We also found no significant correlations of accuracy in the shape discrimination task with the volume of lesions of either the SP or the IPS (all P ’s ≥ 0.285), further suggesting that the decrement in the shape discrimination accuracy is best attributed to forgetting rather than to a lesion of a specific area.…”

“…To limit possible forgetting of the other two tasks, the shape-only sessions were given for no more than three consecutive days. Together with our earlier report (Acerbo et al, 2012 ), these results strongly imply that the Rt may not be directly involved in color discrimination despite the presence of color-sensitive cells (Wang et al, 1993 ). All nine birds were exposed to the shape-only sessions for an average of 38 days, ranging from 4 to 63 days.…”

Systematic Analysis of Pigeons’ Discrimination of Pixelated Stimuli: A Hierarchical Pattern Recognition System Is Not Identifiable

“…22). The optic nerves of birds, already originating in a neurally comparatively rich retina terminate in the optic tecta (TeO) of the mesencephalon, which in turn project mainly to the diencephalic nucleus rotundus (Rt) 67 , which again projects to the voluminous entopallium (E, former ektostriatum) of the telencephalon. It is reasonable to expect that the main stages of visual pattern recognition of birds take place there; the retino-thalamic-telencephalic projection system, so prominent in mammals, is far less prominent in birds 68 .…”