Tectal microcircuit generating visual selection commands on gaze-controlling neurons

Abstract

The optic tectum (called superior colliculus in mammals) is critical for eye-head gaze shifts as we navigate in the terrain and need to adapt our movements to the visual scene. The neuronal mechanisms underlying the tectal contribution to stimulus selection and gaze reorientation remains, however, unclear at the microcircuit level. To analyze this complex-yet phylogenetically conservedsensorimotor system, we developed a novel in vitro preparation in the lamprey that maintains the eye and midbrain intact and allows for whole-cell recordings from prelabeled tectal gaze-controlling cells in the deep layer, while visual stimuli are delivered. We found that receptive field activation of these cells provide monosynaptic retinal excitation followed by local GABAergic inhibition (feedforward). The entire remaining retina, on the other hand, elicits only inhibition (surround inhibition). If two stimuli are delivered simultaneously, one inside and one outside the receptive field, the former excitatory response is suppressed. When local inhibition is pharmacologically blocked, the suppression induced by competing stimuli is canceled. We suggest that this rivalry between visual areas across the tectal map is triggered through long-range inhibitory tectal connections. Selection commands conveyed via gazecontrolling neurons in the optic tectum are, thus, formed through synaptic integration of local retinotopic excitation and global tectal inhibition. We anticipate that this mechanism not only exists in lamprey but is also conserved throughout vertebrate evolution.optic tectum | superior colliculus | GABAergic inhibition | gaze control | evolution V isual scenes are composed of abundant stimuli, and the gaze needs continuously to be redirected toward different objectsan important task for the brain. Current models postulate that stimulus selection occurs through a process involving competitive interaction between different visual stimuli, resulting in the appropriate eye-head movement (1-5). The optic tectum (superior colliculus in mammals) has a causal role in the stimulus selection process (6-12) and not only in the control of saccades and eyehead gaze shifts (13-16). Although the collicular contribution to the selection process is of central importance, the underlying neuronal processes have remained elusive due to methodological limitations. It is our aim here to address this issue in a novel experimental model.The optic tectum is well developed in the lamprey, belonging to the oldest extant vertebrate group that evolved 560 million years ago (17), and it has remained conserved throughout vertebrate phylogeny (18)(19)(20)(21)(22). Afferents from retina provide a direct input to the superficial layers of the optic tectum, where a retinotopic map is formed (23-26). The intermediate and deep layers give rise to projections to brainstem areas and a motor map is formed that is responsible for the coordination of eye, head, and body movements (22,(27)(28)(29).To uncover the mechanisms underlying visual stimulus selection for gaz...

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

“…Application of biccuculine, a GABA A receptor antagonist, enhanced these responses, resulting in robust bursts of action potentials, similar to those observed in vivo during saccades. These results, together with anatomical experiments (Behan & Appell 1992, Kardamakis et al 2015, Lee & Hall 1995, Mooney et al 1988a, Rhoades et al 1989, Tardif et al 2005), now provide solid evidence for the existence of a disynaptic pathway from the retina to the motor layer neurons. This pathway may underlie the generation of ultrafast, express saccades.…”

Complex and spatially segregated auditory inputs of the mouse superior colliculus

“…The presence of the polysynaptic inhibition is perhaps not surprising as feed‐forward inhibition is a common feature of input circuitry in many brain areas and was also described in the superficial and intermediate SC layers (Saito & Isa, ; Kardamakis et al . ). It is likely performed by the fast‐spiking population of neurons in the SGP, as they are known to be GABAergic in the SGI (Sooksawate et al .…”

A hard-wired priority map in the superior colliculus shaped by asymmetric inhibitory circuitry

“…In all vertebrate species studies so far, the superficial, visuosensory layers perform the first step of integrating visual information for the guidance of attention and orienting movements (Kardamakis et al 2015;Vanegas 1984). Indeed, recent work in the rat is consistent with a role for the SC in attention (Clements et al 2014;Mitchinson and Prescott 2013).…”

“…Whether hard-wired intrinsic circuits contribute to such functions is unknown. Because the vertebrate SC is known to mediate orienting behaviors and to play a role in target selection (Carello and Krauzlis 2004;Horwitz and Newsome 2001;Kardamakis et al 2015;Krauzlis et al 2013), we explored the network activity along the amplitude-encoding axis of the SC of the rat. SC slices cut in the parasagittal plane isolated this circuitry, and voltage imaging (Cohen and Salzberg 1978) revealed a surprising and very strong bias in the spread of responses to electrical stimulation, in some instances extending Ͼ3-fold further in the caudal direction than in the rostral direction.…”