Space-Specific Deficits in Visual Orientation Discrimination Caused by Lesions in the Midbrain Stimulus Selection Network

Abstract

Summary Perceptual decisions require both analysis of sensory information and selective routing of relevant information to decision networks. This study explores the contribution of a midbrain network to visual perception in chickens. Analysis of visual orientation information in birds takes place in the forebrain sensory area called the Wulst, as it does in the primary visual cortex (V1) of mammals. In contrast, the midbrain, which receives parallel retinal input, encodes orientation poorly, if at all. We discovered, however, that small electrolytic lesions in the midbrain severely impair a chicken’s ability to discriminate orientations. Focal lesions were placed in the optic tectum (OT) and in the nucleus isthmi pars parvocellularis (Ipc) – key nodes in the midbrain stimulus selection network – in chickens trained to perform an orientation discrimination task. A lesion in the OT caused a severe impairment in orientation discrimination specifically for targets at the location in space represented by the lesioned location. Distracting stimuli increased the deficit. A lesion in the Ipc produced similar but more transient effects. We discuss the possibilities that performance deficits were caused by interference with orientation information processing (sensory deficit) versus with the routing of information in the forebrain (agnosia). The data support the proposal that the OT transmits a space specific signal that is required to gate orientation information from the Wulst into networks that mediate behavioral decisions, analogous to the role of ascending signals from the SC in monkeys. Furthermore, our results indicate a critical role for the cholinergic Ipc in this gating process.

Evolution of neural processing for visual perception in vertebrates

“…However, none of the lesion-behavior studies have tested for the ability of birds to discriminate among values of specific spatial features (i.e., among different orientations, distances, or directions of motion). Behavioral paradigms and stimuli that enable such measurements have now been developed (Knudsen, Schwarz, Knudsen, & Sridharan, 2017;Nguyen et al, 2004;Nieder & Wagner, 2001). Future experiments should apply these techniques to test threshold discrimination performance in birds with lesions in the retinogeniculate pathway.…”

“…Most lesion studies could not distinguish deficits caused by agnosia (attention deficit) from those caused by the loss of the visual information per se (Cook et al, ; Nguyen et al, ; Watanabe et al, ). However, one OT lesion study has demonstrated agnosia for line orientations, a feature value that is processed in the Wulst (Knudsen et al, ). The inability of birds to discriminate line orientations following OT lesions indicates that OT attention signals gate not only visual information that is transmitted to the forebrain via the retinotectal pathway, but also gate information that is transmitted to the forebrain via the retinogeniculate pathway, as is true also for the SC in mammals (Krauzlis et al, ; Sridharan et al, ).…”

“…Because the functional properties of neurons in the nucleus rotundus and entopallium are likely to be dramatically modulated by attention, and because they have not been studied previously in behaving birds, the full extent of their coding capabilities remains unknown. In the future, it will be essential to study the properties of these neurons in behaving birds using paradigms that control attention (Knudsen et al, ).…”

Neural Circuits That Mediate Selective Attention: A Comparative Perspective

“…In birds, space-specific top-down signals, by facilitating sensory responses to a particular location, shift the balance of competition to favor the location signaled by the forebrain [42]. Conversely, focal inactivation of the Ipc or OT prevents any stimulus at the represented location from being selected as “highest priority,” even when there are no competing stimuli [43].…”

“…This selection signal spatially filters visual information within the OT as well as in the forebrain (Fig. 2D) [43].…”