Expression patterns of ion channels and structural proteins in a multimodal cell type of the avian optic tectum

Abstract

The midbrain is an important subcortical area involved in distinct functions such as multimodal integration, movement initiation, bottom-up, and top-down attention. Our group is particularly interested in cellular computation of multisensory integration. We focus on the visual part of the avian midbrain, the optic tectum (TeO, counterpart to mammalian superior colliculus). This area has a layered structure with the great advantage of distinct input and output regions. In chicken, the TeO is organized in 15 layers where visual input targets the superficial layers while auditory input terminates in deeper layers. One specific cell type, the Shepherd's crook neuron (SCN), extends dendrites in both input regions. The characteristic feature of these neurons is the axon origin at the apical dendrite. The molecular identity of this characteristic region and thus, the site of action potential generation are of particular importance to understand signal flow and cellular computation in this neuron. We present immunohistochemical data of structural proteins (NF200, Ankyrin G, and Myelin) and ion channels (Pan-Na , Na 1.6, and K 3.1b). NF200 is strongly expressed in the axon. Ankyrin G is mainly expressed at the axon initial segment (AIS). Myelination starts after the AIS as well as the distribution of Na channels on the axon. The subtype Na 1.6 has a high density in this region. K 3.1b is restricted to the soma, the primary neurite and the axon branch. The distribution of functional molecules in SCNs provides insight into the information flow and the integration of sensory modalities in the TeO of the avian midbrain.

“Shepherd’s crook” neurons drive and synchronize the enhancing and suppressive mechanisms of the midbrain stimulus selection network

“…This common innervation explains the synchrony between bursting events in the Ipc and the Imc and also between bursts in the Ipc and spikes in SLu reported in pigeons (13). From a computational point of view, the results suggest that Shc neurons may perform as "operational" hubs (28): While receiving retinal inputs in their apical dendrites as well as other inputs in their deeper dendrites (18), they drive and synchronize three concurrent neural processes, each with different functions and spike-firing profiles. We will argue that this feat could be attained by marked differences in axonal convergence, varying degrees of synchrony between Shc neurons, and postsynaptic mechanisms.…”

“…The peculiar bipolar morphology of Shc neurons would facilitate this integration, as their apical dendrites could summate visual inputs from different types of retinal ganglion cell terminals. The deep dendrites could add up auditory inputs arriving on deeper tectal layers (18,39) and also top-down influences from the arcopallium, which are able to bias the competing interactions within the isthmotectal system (31,40). The arcopallium can induce saccadic eye movements through a direct pathway to brainstem oculomotor centers and has been compared with the mammalian frontal eye fields (41); thus, Shcs may link stimulus selection to saccades, initiated by both pallial and mesencephalic circuits.…”

“…A central node of the avian midbrain selection network is the "shepherd's-crook" neurons (Shc) ( Fig. 1) (17,18), which relay retinal inputs arriving to the superficial tectal layers to the nuclei isthmi pars parvocellularis (Ipc), pars semilunaris (SLu), and pars magnocellularis (Imc) (16,19). Neurons from Ipc and SLu send reentrant signals via columnar axons that terminate in the same tectal position from which the visual input originates (16,20,21).…”

Neuron types in the zebrafish optic tectum labeled by an id2b transgene

“…These neurons formed bushy, nonstratified dendrites restricted to the deep SGC and SAC layers of the tectal neuropil, similar to those we have previously described for dlx5/6‐ positive tectal projection neurons (Figure a–d; Robles et al, ). A feature we commonly observed in TGPNs was a discrete “shepherd's crook,” where the primary dendrite formed an apically oriented loop that gave rise to the descending, extratectal neurite process (Lischka, Ladel, Luksch, & Weigel, ; arrows in Figure b,d). This long neurite extended laterally in the tectal NP to exit tectum ventrally, via the tectobulbar tract (Sato, Hamaoka, Aizawa, Hosoya, & Okamoto, ).…”

“…In addition, TLPNs that innervated the contralateral TL had cell bod- Robles et al, 2011). A feature we commonly observed in TGPNs was a discrete "shepherd's crook," where the primary dendrite formed an apically oriented loop that gave rise to the descending, extratectal neurite process (Lischka, Ladel, Luksch, & Weigel, 2018; arrows in Figure 9b,d). This long neurite extended laterally in the tectal NP to exit tectum ventrally, via the tectobulbar tract (Sato, F I G U R E 7 A population of id2b:gal4 positive tectal neurons forms a topographic projection to torus longitudinalis.…”