Columnar projections from the cholinergic nucleus isthmi to the optic tectum in chicks (Gallus gallus): A possible substrate for synchronizing tectal channels

Abstract

The cholinergic division of the avian nucleus isthmi, the homolog of the mammalian nucleus parabigeminalis, is composed of the pars parvocellularis (Ipc) and pars semilunaris (SLu). Ipc and SLu were studied with in vivo and in vitro tracing and intracellular filling methods. 1) Both nuclei have reciprocal homotopic connections with the ipsilateral optic tectum. The SLu connection is more diffuse than that of Ipc. 2) Tectal inputs to Ipc and SLu are Brn3a-immunoreactive neurons in the inner sublayer of layer 10. Tectal neurons projecting on Ipc possess "shepherd's crook" axons and radial dendritic fields in layers 2-13. 3) Neurons in the mid-portion of Ipc possess a columnar spiny dendritic field. SLu neurons have a large, nonoriented spiny dendritic field. 4) Ipc terminals form a cylindrical brush-like arborization (35-50 microm wide) in layers 2-10, with extremely dense boutons in layers 3-6, and a diffuse arborization in layers 11-13. SLu neurons terminate in a wider column (120-180 microm wide) lacking the dust-like boutonal features of Ipc and extend in layers 4c-13 with dense arborizations in layers 4c, 6, and 9-13. 5) Ipc and SLu contain specialized fast potassium ion channels. We propose that dense arborizations of Ipc axons may be directed to the distal dendritic bottlebrushes of motion detecting tectal ganglion cells (TGCs). They may provide synchronous activation of a group of adjacent bottlebrushes of different TGCs of the same type via their intralaminar processes, and cross channel activation of different types of TGCs within the same column of visual space.

Attentional Capture? Synchronized Feedback Signals from the Isthmi Boost Retinal Signals to Higher Visual Areas

“…First, they lasted for 2 ms with a clear biphasic profile characteristic of soma recordings. Second, their RFs' position followed the retinotopic map described for the nucleus Wang et al, 2006), with superior to inferior shifts in RF position (in the visual field) as the electrode moved from lateral to medial in the nu- cleus, and posterior to anterior shifts in RF position as the electrode moved from posterior to anterior in the nucleus. Large changes in RF position occurred for short displacements of the electrodes, in accordance with the small size of the nucleus.…”

“…As shown in Figure 1, the Ipc and SLu have a remarkably similar connectivity, both receiving a topographic projection from shepherd-crook neurons in tectal layer ten, and a non-topographic projection from the Imc neurons, the last consisting of large axonal fields ramifying extensively in each nucleus (Wang et al, 2006). Extracellular recordings in the Ipc reveal this dual input: Ipc neurons respond with bursting discharges from circumscribed RFs, while the Imc terminals respond with synchronized barrages of spikes, which can be elicited by stimulating most parts of the visual field (Marín et al, 2007).…”

“…A retinal input arriving at the superficial tectal layers will activate a local feedback response from the Ipc and SLu (in red), and a widespread inhibition in the TeO, Ipc, and SLu mediated by the activation of Imc neurons (in blue). Activated TGCs will transmit this visual activity to the corresponding divisions in the Rt (adapted with permission from Wang et al, 2006). recording of simultaneous responses in all structures with a single moving stimulus.…”

“…The optic tectum is reciprocally connected with three nuclei in the isthmic complex, the nucleus isthmi pars magnocellularis (Imc), pars parvocellularis (Ipc), and pars semilunaris (SLu), each of which receives a prominent visual projection from neurons in tectal layer ten (Hunt et al, 1977;Güntürkün and Remy, 1990;Wang et al, 2004;Wang et al, 2006). Imc neurons have large GABAergic terminal fields providing wide-field inhibition throughout Ipc, SLu, and the deep layers of TeO (Wang et al, 2004;Marín et al, 2007).…”

“…Imc neurons have large GABAergic terminal fields providing wide-field inhibition throughout Ipc, SLu, and the deep layers of TeO (Wang et al, 2004;Marín et al, 2007). Ipc and SLu neurons project back to TeO in a precise homotopic fashion, via columnar axons that densely ramify in complementary layers (Wang et al, 2006). It has been proposed that this complementary arrangement could differentially control the ascending visual streams mediated by the different TGC classes, each class projecting to specific Rt subdivisions (Wang et al, 2006) (Fig.…”