Optogenetic investigation of the role of the superior colliculus in orienting movements

Abstract

In vivo studies have demonstrated that the superior colliculus (SC) integrates sensory information and plays a role in controlling orienting motor output. However, how the complex microcircuitry within the SC, as documented by slice studies, subserves these functions is unclear. Optogenetics affords the potential to examine, in behaving animals, the functional roles of specific neuron types that comprise heterogeneous nuclei. As a first step toward understanding how SC microcircuitry underlies motor output, we applied optogenetics to mice performing an odor discrimination task in which sensory decisions are reported by either a leftward or rightward SC-dependent orienting movement. We unilaterally expressed either channelrhodopsin-2 or halorhodopsin in the SC and delivered light in order to excite or inhibit motor-related SC activity as the movement was planned. We found that manipulating SC activity predictably affected the direction of the selected movement in a manner that depended on the difficulty of the odor discrimination. This study demonstrates that the SC plays a similar role in directional orienting movements in mice as it does in other species, and provides a framework for future investigations into how specific SC cell types contribute to motor control.

Segregated fronto‐cortical and midbrain connections in the mouse and their relation to approach and avoidance orienting behaviors

“…In rats, appetitive hunting and whisking behavior results in increased c‐FOS expression within the SCl, and lesions of the SCl decrease predatory orienting behaviors (Favaro et al, 2011; Furigo et al, 2010). Research groups who investigate auditory or odor cued orienting responses in the SC often place probes (electrodes, optrodes) in the lateral portion of the SC (Duan, Erlich, & Brody, 2015; Felsen & Mainen, 2012; Stubblefield, Costabile, & Felsen, 2013), and thus our knowledge regarding stimulus processing in the mouse SC might be biased toward appetitive stimulus types. Once processed, the SCl sends the information through the crossed tecto‐reticulo‐spinal tract to brain stem motor nuclei to initiate approach behavior (Redgrave, Dean, & Westby, 1990).…”

An integrative role for the superior colliculus in selecting targets for movements

“…Indeed, studies that have manipulated the activity of one group of SC neurons-presumably corresponding to one of the targetshave indeed observed a larger effect on difficult than on easy trials (Fig. 3;McPeek and Keller 2004;Song et al 2011;Stubblefield et al 2013;Thevarajah et al 2009). Other studies have taken advantage of the known topographic representation of target locations in the SC to demonstrate that inactivating neurons representing one location biases target selection away from the inactivated locus (McPeek and Keller 2004;Krauzlis 2010, 2011).…”

“…These studies showed that the activity of many SNr neurons is modulated well before movement initiation (Handel and Glimcher 1999), depends on the magnitude of reward associated with the movement A: unilateral channelrhodopsin-2 (ChR2)-mediated optical activation in the SC has a greater effect (contraversive shift) on hard trials (small odor mixture contrasts) than easy trials (large odor contrast). Data from Stubblefield et al (2013). B: unilateral inhibition via muscimol infusion into the SC has a greater effect (ipsiversive shift) on hard trials than easy trials.…”

Activity in mouse pedunculopontine tegmental nucleus reflects action and outcome in a decision-making task

“…Details of the behavioral training protocol are described by Stubblefield et al (2013). Briefly, after acclimation to 5 days of water restriction (1 ml of water per day), all mice were trained to perform the odor-cued spatial choice task with the following initial stages.…”