A specialized reciprocal connectivity suggests a link between the mechanisms by which the superior colliculus and parabigeminal nucleus produce defensive behaviors in rodents

Abstract

The parabigeminal nucleus (PBG) is the mammalian homologue to the isthmic complex of other vertebrates. Optogenetic stimulation of the PBG induces freezing and escape in mice, a result thought to be caused by a PBG projection to the central nucleus of the amygdala. However, the isthmic complex, including the PBG, has been classically considered satellite nuclei of the Superior Colliculus (SC), which upon stimulation of its medial part also triggers fear and avoidance reactions. As the PBG-SC connectivity is not well characterized, we investigated whether the topology of the PBG projection to the SC could be related to the behavioral consequences of PBG stimulation. To that end, we performed immunohistochemistry, in situ hybridization and neural tracer injections in the SC and PBG in a diurnal rodent, the Octodon degus. We found that all PBG neurons expressed both glutamatergic and cholinergic markers and were distributed in clearly defined anterior (aPBG) and posterior (pPBG) subdivisions. The pPBG is connected reciprocally and topographically to the ipsilateral SC, whereas the aPBG receives afferent axons from the ipsilateral SC and projected exclusively to the contralateral SC. This contralateral projection forms a dense field of terminals that is restricted to the medial SC, in correspondence with the SC representation of the aerial binocular field which, we also found, in O. degus prompted escape reactions upon looming stimulation. Therefore, this specialized topography allows binocular interactions in the SC region controlling responses to aerial predators, suggesting a link between the mechanisms by which the SC and PBG produce defensive behaviors.

Unraveling circuits of visual perception and cognition through the superior colliculus

“…These neuronal responses are presumably subject to modulation as a looming stimulus can induce both rapid escape and freezing, depending on environmental context like the presence of a shelter (Vale et al, 2017) or stimulus parameters such as loom speed and size (Yang et al, 2020). A highly visual diurnal rodent, the com-mon degu (Octodon degus), also shows looming-evoked escape (Deichler et al, 2020). In mice, superficial layer neurons respond to visual looming (Zhao et al, 2014), and optogenetic inhibition of the excitatory SC neurons in the medial region of the intermediate layer reduces looming-induced freezing (Wei et al, 2015).…”

Cell type‐ and layer‐specific convergence in core and shell neurons of the dorsal lateral geniculate nucleus

“…We found monosynaptic inputs from the PBG to the shell, but not from the PBG or PPT to the dLGN core, suggesting that neurons in the PBG provide inputs to neurons in the dLGN shell, but not to excitatory relay neurons in the dLGN core. The PBG has been reported to receive retinal inputs from ON–OFF DS‐GCs and alpha‐RGCs (Reinhard et al, 2019) and be involved in innate and visual defensive responses, such as escape and freezing (Deichler et al, 2020). We found that the shell dLGN receives inputs from the ipsilateral sSC and contralateral PBG.…”

“…Our finding is consistent with those of a study indicating that both the parabigemino‐genuculate projections and tecto‐genuculate projections to the dLGN terminate in the shell region containing W‐like cells (Harting, Van Lieshout, et al, 1991). The interactions between the SC, PBG, and dLGN might be important for visually guided avoidance behaviors (Deichler et al, 2020).…”

Nonlinear visuoauditory integration in the mouse superior colliculus

“…However, we did not identify the source of this modulation in this study. Potential sources include local circuitry within the SC 21 , 28 , a pathway with higher latency such as a cortical pathway 29 , and/or reciprocal connections with other brain areas such as the parabigeminal nucleus [30][31][32] .…”