Active Dendritic Properties and Local Inhibitory Input Enable Selectivity for Object Motion in Mouse Superior Colliculus Neurons

Abstract

Neurons respond to specific features of sensory stimuli. In the visual system, for example, some neurons respond to motion of small but not large objects, whereas other neurons prefer motion of the entire visual field. Separate neurons respond equally to local and global motion but selectively to additional features of visual stimuli. How and where does response selectivity emerge? Here, we show that wide-field (WF) cells in retino-recipient layers of the mouse superior colliculus (SC) respond selectively to small moving objects. Moreover, we identify two mechanisms that contribute to this selectivity. First, we show that input restricted to a small portion of the broad dendritic arbor of WF cells is sufficient to trigger dendritic spikes that reliably propagate to the soma/axon. In vivo whole-cell recordings reveal that nearly every action potential evoked by visual stimuli has characteristics of spikes initiated in dendrites. Second, inhibitory input from a different class of SC neuron, horizontal cells, constrains the range of stimuli to which WF cells respond. Horizontal cells respond preferentially to the sudden appearance or rapid movement of large stimuli. Optogenetic reduction of their activity reduces movement selectivity and broadens size tuning in WF cells by increasing the relative strength of responses to stimuli that appear suddenly or cover a large region of space. Therefore, strongly propagating dendritic spikes enable small stimuli to drive spike output in WF cells and local inhibition helps restrict responses to stimuli that are both small and moving.

The nucleus pretectalis principalis: A pretectal structure hidden in the mammalian thalamus

“…The SZ receives projections from the parabigeminal nucleus (PBG) (Graybiel, ), the proposed homolog of the avian Ipc (Gruberg et al, ). In addition, horizontal interneurons cover the SZ with GABA‐rich processes (Gale & Murphy, , ). Physiological evidence indicates these neurons directly contact and exert a strong inhibitory modulation on the TGC activity (Gale & Murphy, ).…”

“…In addition, horizontal interneurons cover the SZ with GABA‐rich processes (Gale & Murphy, , ). Physiological evidence indicates these neurons directly contact and exert a strong inhibitory modulation on the TGC activity (Gale & Murphy, ). Our results add Pul‐T cells to the sources of GABA (and NPY) in the SZ.…”

“…Most of the units recorded in the Rt and TGCs exhibit complex, higher order motion sensitivity responses, such as two‐dimensional and in‐depth motion (Wang, Jiang, & Frost, ; Wang & Frost, ). Likewise, in single cell recordings, TGCs in the mouse SC selectively respond to small bi‐dimensional moving disks and to looming stimuli (Gale & Murphy, , ). Therefore, it can be expected that PT also exhibits, and participate in the modulation of, motion sensitivity at the tectal level.…”

Circuits for Action and Cognition: A View from the Superior Colliculus

“…Similarly, when multiple stimuli appear and one is in a collicular neuron’s response field and one is outside of the response field, even in the opposite hemifield, the discharge rate is reduced, compared to when a stimulus is presented in the preferred location alone (Basso & Wurtz 1997, 1998; Rizzolatti et al 1973, 1974). Collicular neurons also show suppressed activity with increases in the size of a visual stimulus (Gale & Murphy 2016, Goldberg & Wurtz 1972a) and show averaged rather than summed levels of activity when two stimuli appear in individual response fields (Li & Basso 2005). The results from these studies indicate that signals generated by visual input to the colliculus may be integrated within the colliculus through a process of normalization.…”

The mouse pulvinar nucleus: Organization of the tectorecipient zones

“…However, the availability of transgenic mouse lines (e.g. Byun et al, 2016; Gale and Murphy, 2014, 2016) may help to facilitate the categorization of these cells. If subclasses of WFV cells exist in the mouse, those that extend dendrites most superficially within the SC (Figure 2C) could potentially be innervated by populations of retinal axons that are restricted to the most superficial regions of the SGS (e.g.…”