"Shepherd's crook" neurons drive and synchronize the enhancing and suppressive mechanisms of the midbrain stimulus selection network.

The optic tectum (TeO), or superior colliculus, is a multisensory midbrain center that organizes spatially orienting responses to relevant stimuli. To define the stimulus with the highest priority at each moment, a network of reciprocal connections between the TeO and the isthmi promotes competition between concurrent tectal inputs. In the avian midbrain, the neurons mediating enhancement and suppression of tectal inputs are located in separate isthmic nuclei, facilitating the analysis of the neural processes that mediate competition. A specific subset of radial neurons in the intermediate tectal layers relay retinal inputs to the isthmi, but at present it is unclear whether separate neurons innervate individual nuclei or a single neural type sends a common input to several of them. In this study, we used in vitro neural tracing and cell-filling experiments in chickens to show that single neurons innervate, via axon collaterals, the three nuclei that comprise the isthmotectal network. This demonstrates that the input signals representing the strength of the incoming stimuli are simultaneously relayed to the mechanisms promoting both enhancement and suppression of the input signals. By performing in vivo recordings in anesthetized chicks, we also show that this common input generates synchrony between both antagonistic mechanisms, demonstrating that activity enhancement and suppression are closely coordinated. From a computational point of view, these results suggest that these tectal neurons constitute integrative nodes that combine inputs from different sources to drive in parallel several concurrent neural processes, each performing complementary functions within the network through different firing patterns and connectivity.

Axon terminals from the nucleus isthmi pars parvocellularis control the ascending retinotectofugal output through direct synaptic contact with tectal ganglion cell dendrites.

The optic tectum in birds and its homologue the superior colliculus in mammals both send major bilateral, nontopographic projections to the nucleus rotundus and caudal pulvinar, respectively. These projections originate from widefield tectal ganglion cells (TGCs) located in layer 13 in the avian tectum and in the lower superficial layers in the mammalian colliculus. The TGCs characteristically have monostratified arrays of brush-like dendritic terminations and respond mostly to bidimensional motion or looming features. In birds, this TGC-mediated tectofugal output is controlled by feedback signals from the nucleus isthmi pars parvocellularis (Ipc). The Ipc neurons display topographically organized axons that densely ramify in restricted columnar terminal fields overlapping various neural elements that could mediate this tectofugal control, including the retinal terminals and the TGC dendrites themselves. Whether the Ipc axons make synaptic contact with these or other tectal neural elements remains undetermined. We double labeled Ipc axons and their presumptive postsynaptic targets in the tectum of chickens (Gallus gallus) with neural tracers and performed an ultrastructural analysis. We found that the Ipc terminal boutons form glomerulus-like structures in the superficial and intermediate tectal layers, establishing asymmetric synapses with several dendritic profiles. In these glomeruli, at least two of the postsynaptic dendrites originated from TGCs. We also found synaptic contacts between retinal terminals and TGC dendrites. These findings suggest that, in birds, Ipc axons control the ascending tectal outflow of retinal signals through direct synaptic contacts with the TGCs.

The isthmic nuclei providing parallel feedback connections to the avian tectum have different neurochemical identities: Expression of glutamatergic and cholinergic markers in the chick (Gallus gallus).

Retinal inputs to the optic tectum (TeO) triggered by moving stimuli elicit synchronized feedback signals from two isthmic nuclei: the isthmi parvocelullaris (Ipc) and isthmi semilunaris (SLu). Both of these nuclei send columnar axon terminals back to the same tectal position receiving the retinal input. The feedback signals from the Ipc seem to act as an attentional spotlight by selectively boosting the propagation of retinal inputs from the tectum to higher visual areas. Although Ipc and SLu nuclei are widely considered cholinergic because of their immunoreactivity for choline acetyltransferase (ChAT), contradictory findings, including the expression of the vesicular glutamate transporter 2 (VGluT2) mRNA in Ipc neurons, have raised doubts about the purely cholinergic nature of this nucleus. In this study, in chicks, we revise the neurochemical identity of the isthmic nuclei by using in situ hybridization assays for VGluT2 along with three cholinergic markers: the vesicular acetylcholine transporter (VAChT), the high-affinity choline transporter (CHT1) and ChAT. We found that neurons in the SLu showed strong mRNA expression of all three cholinergic markers, whereas the expression of VAChT mRNA in the Ipc was undetectable in our essays. Instead, Ipc neurons exhibited a strong expression of VGluT2 mRNA. Immunohistochemistry assays showed VGluT2 immunoreactivity in the TeO codistributing with anterogradely labeled Ipc axon-terminal boutons, further supporting a glutamatergic function for the Ipc nucleus. Therefore, our results strongly suggest that, in the chick, whereas the feedback from the SLu to the TeO is indeed cholinergic, the feedback from the Ipc has a marked glutamatergic component.