Expression patterns of ion channels and structural proteins in a multimodal cell type of the avian optic tectum
The midbrain is an important subcortical area. It is involved in many functions such as integrating different sensory modalities, movement initiation, bottom‐up attention caused by the isthmic system and top‐down attention mediated by hyperpallial projections (Karten, Cox, & Mpodozis, 1997; Miceli, Repérant, Bavikati, Rio, & Volle, 1997; Knudsen, Cohen, & Masino, 1995; Luksch, 2003; Knudsen, 2007; Wylie, Gutierrez‐Ibanez, Pakan, & Iwaniuk, 2009; Sridharan & Knudsen, 2015). The avian midbrain is subdivided in a visual dominated part, the optic tectum (TeO, counterpart to the superior colliculus in mammals) and an auditory dominated part, the nucleus mesencephalicus lateralis pars dorsalis (MLd, counterpart to the inferior colliculus). The avian optic tectum integrates topographic, multimodal sensory information into a multisensory map of space, which is dominated by the visual modality (Knudsen, 1982; Meredith & Stein, 1986; Witten & Knudsen, 2005). The visual signal is processed by retinal ganglion cells (RGCs) projecting from the retina to the stratum opticum (SO, layer 1 of the optic tectum) and terminate in retinorecipient laminae 2 to 5 and 7 (Mey & Thanos, 2000; Yamagata, Weiner, Dulac, Roth, & Sanes, 2006). Incoming visual information is integrated by tectal cells to generate responses to luminance, motion and direction (Jassik‐Gerschenfeld & Guichard, 1972; Luksch, Khanbabaie, & Wessel, 2004; Verhaal & Luksch, 2016), and passed on toward higher brain regions (Luksch, 2003). In addition to visual information, an auditory map of space is found in the TeO (Knudsen, 1982). In chicken, the auditory signal is processed from the brainstem to two interconnected structures in the midbrain: the MLd and the TeO. The external part of the inferior colliculus (ICx) relays the auditory information either directly to the deeper layers of the optic tectum (Pena & Gutfreund, 2014) or across an external portion of the formatio reticularis lateralis (FRLx; Niederleitner, Gutierrez‐Ibanez, Krabichler, Weigel, & Luksch, 2017; Niederleitner & Luksch, 2012).
The TeO is composed of 15 layers, each of which can be characterized by its cell‐type specific appearance and connectivity (Luksch, 2003). An advantage of this layered layout is the strict distinction into input and output layers, which allows to study physiological properties and signal propagation in layer‐specific neurons. Despite the findings of different sensory maps of space, little is known about the multimodal integration on subcellular level. A candidate for multimodal integration is the Shepherd's crook neuron (SCN), a cell type in layer 10 of the TeO of chicken. It has dendrites in retinorecipient layers and deeper layers, respectively. The axon of this neuron has a unique morphology, as it branches from the apical dendrite and immediately turns downwards in a characteristic curve to the deeper layers to terminate in the isthmic nuclei (Luksch, 2003). The isthmic nuclei form a reciprocal network with the optic tectum which is involved in bottom‐up attention (Goddard, Mysore, Bryant, Huguenard, & Knudsen, 2014; Lai, Brandt, Luksch, & Wessel, 2011; Meyer et al., 2008; Wang, Luksch, Brecha, & Karten, 2006). Interestingly, units in the isthmic nuclei respond to both visual and auditory input (Maczko, Knudsen, & Knudsen, 2006). Since SCNs are the only neurons projecting to the isthmic nuclei (Marin, Mpodozis, Sentis, Ossandon, & Letelier, 2005; Wang et al., 2006), these findings strengthen the hypothesis that SCN neurons integrate multimodal input.
The SCN had first been described by Ramón y Cajal (1909) who suggested direct information flow from visual input onto the axon, without prior integration in the neuronal soma. In this study, we critically assess this hypothesis by studying molecular markers usually expressed in the axonal initiation zone.