Exploring the Superior Colliculus In Vitro

Abstract

The superior colliculus plays an important role in the translation of sensory signals that encode the location of objects in space into motor signals that encode vectors of the shifts in gaze direction called saccades. Since the late 1990s, our two laboratories have been applying whole cell patch-clamp techniques to in vitro slice preparations of rodent superior colliculus to analyze the structure and function of its circuitry at the cellular level. This review describes the results of these experiments and discusses their contributions to our understanding of the mechanisms responsible for sensorimotor integration in the superior colliculus. The experiments analyze vertical interactions between its superficial visuosensory and intermediate premotor layers and propose how they might contribute to express saccades and to saccadic suppression. They also compare and contrast the circuitry within each of these layers and propose how this circuitry might contribute to the selection of the targets for saccades and to the build-up of the premotor commands that precede saccades. Experiments also explore in vitro the roles of extrinsic inputs to the superior colliculus, including cholinergic inputs from the parabigeminal and parabrachial nuclei and GABAergic inputs from the substantia nigra pars reticulata, in modulating the activity of the collicular circuitry. The results extend and clarify our understanding of the multiple roles the superior colliculus plays in sensorimotor integration.

Order of operations for decoding superior colliculus activity for saccade generation

“…However, it is important to recognize that ascending outputs of the SC could also contribute to the transformation. For example, stimulation of the deep layers could activate neurons in the superficial layers (Isa and Hall 2009;Vokoun et al 2010), which in turn could recruit the intraparietal cortex via the pulvinar (Clower et al 2001). Neurons in the deep SC layers could also recruit the frontal eye fields (FEFs) via the mediodorsal thalamus (Sommer and Wurtz 2004).…”

Similarity of superior colliculus involvement in microsaccade and saccade generation

“…Through local excitation, this differential activation could get amplified and gradually lead to elevated firing rates until a movement is triggered. Alternately, modulation of inhibitory input (e.g., from substantia nigra; Hikosaka and Wurtz 1985;Isa and Hall 2009;Liu and Basso 2008) or excitatory input (e.g., from the prefrontal cortex; Sommer and Wurtz 2000;Wurtz et al 2001) could shape SC population activity and contribute to microsaccade-related buildup. These mechanisms are sources of saccade-related buildup of activity elsewhere in the SC, highlighting the similarity between microsaccades and saccades at the mechanistic level.…”

Tectal microcircuit generating visual selection commands on gaze-controlling neurons

“…Although most mammalian studies have focused on the role of the retinotopic excitatory circuits that mediate signal transmission between the superficial layer and the deeper layers (33)(34)(35)(36), only more recent studies have emphasized the role of GABAergic circuits in the collicular control of gaze (37)(38)(39)(40)(41)(42)(43)(44)(45). The question how collicular GABAergic systems affect stimulus selection for gaze motor action has, however, remained unanswered because most studies have relied on extracellular recordings in vivo and therefore have not allowed an analysis of the synaptic basis for these inhibitory interactions.…”