A centrifugally controlled circuit in the avian retina and its possible role in visual attention switching

Abstract

The isthmo-optic nucleus (ION) is the main source of efferents to the retina in birds. Isthmo-optic neurons project in topographical order on amacrine cells in the ventral parts of the retina, and a subclass of these known as proprioretinal neurons project onto the dorsal retina. We propose that, through the intermediary of the amacrine target cells, activity in the isthmo-optic pathway excites ganglion cells locally in the ventral retina but inhibits those in dorsal regions. This circuit would thereby mediate centrifugally controlled switches in attention between the dorsal retina, involved in feeding, and the more ventral parts, involved in scanning for predators. This hypothesis accounts for a wide range of disparate data from behavior, comparative anatomy, endocrinology, hodology, and neurophysiology.

Roots of a social brain: Developmental models of emerging animacy-detection mechanisms

“…It is supposed to play a role in the selective shifting of visual attention in the retina, via a winner-takeall mechanism, during feeding and the control of pecking (Gruberg et al, 2006;Marin et al, 2005Marin et al, , 2007. This selection occurs either between relevant stimuli (Rogers and Miles, 1972;Uchiyama, 1989;Ward et al, 1991;Uchiyama and Barlow, 1994;Uchiyama et al, 1998) or between the ventral and dorsal parts of the retina (Wilson and Lindstrom, 2011;Catsicas et al, 1987;Clarke et al, 1996). Additional hypotheses on the functional role of this pathway include: involvement in the saccadic suppression of retinal activity (Holden, 1968;Nickla et al, 1994), enhancement of peripheral vision (Marin et al, 1990) and modulation of temporal processing (Knipling, 1978).…”

Morphology and Dye-Coupling of Cells in the Pigeon Isthmo-Optic Nucleus

“…The two parts of the retina might be connected by intrinsic interneurons [Woodson et al, 1991] or by the proprioretinal neurons which project long axons from the ventral retina to the dorsal retina. Therefore, local enhancement of the ventral retina and long-range inhibition in the dorsal retina would result in the switching of visual attention switching [Clarke et al, 1996]. Our recent electrophysiological findings [Li et al, 1998] lend strong support to this notion.…”

“…In recent years, accumulating evidence supports the hypothesis that this centrifugal system may act as a 'searchlight' in ground-feeding birds, highlighting or alerting them to threatening targets in the upper visual field [Uchiyama, 1989;Holden, 1990]. In fact, this system has a heterotopic organization: i.e., the ION receives its major input from the dorsal retina via the tectum and projects primarily to the ventral retina [Holden, 1990;Woodson et al, 1995;Clarke et al, 1996]. The two parts of the retina might be connected by intrinsic interneurons [Woodson et al, 1991] or by the proprioretinal neurons which project long axons from the ventral retina to the dorsal retina.…”

“…Several hypotheses have postulated that this nucleus may be involved in visual attention, search, and discrimination [Uchiyama, 1989;Holden, 1990;Clarke et al, 1996]. In recent years, accumulating evidence supports the hypothesis that this centrifugal system may act as a 'searchlight' in ground-feeding birds, highlighting or alerting them to threatening targets in the upper visual field [Uchiyama, 1989;Holden, 1990].…”

“…On the basis of electrophysiological and neuroanatomical findings, some hypotheses concerning the functional significance of centrifugal pathways have been proposed [Uchiyama, 1989;Holden, 1990;Woodson et al, 1995;Clarke et al, 1996]. Within the feedback loop, tectal neurons projecting to ION are located in layer 9 and at the border between layers 9 and 10 of the tectum.…”