Overt Responses during Covert Orienting

Abstract

A distributed network of cortical and subcortical brain areas controls our oculomotor behavior. This network includes the superior colliculus (SC), which coordinates an ancient visual grasp reflex via outputs that ramify widely within the brainstem and spinal cord, accessing saccadic and other premotor and autonomic circuits. In this Review, we discuss recent results correlating subliminal SC activity in the absence of saccades with diverse components of the visual grasp reflex, including neck and limb muscle recruitment, pupil dilation, and microsaccade propensity. Such subtle manifestations of covert orienting are accessible in the motor periphery and may provide the next generation of oculomotor biomarkers in health and disease.

Transcranial Magnetic Stimulation of the Prefrontal Cortex in Awake Nonhuman Primates Evokes a Polysynaptic Neck Muscle Response That Reflects Oculomotor Activity at the Time of Stimulation

“…Importantly, single-pulse TMS to the frontal cortex never evoked a saccadic eye movement, which is consistent with previous reports delivering TMS-FEF in humans (Müri et al, 1991;Wessel and Kömpf, 1991) and NHPs (Valero-Cabre et al, 2012). The ability of low-frequency forms of stimulation to evoke neck muscle responses without saccades likely reflects differences in the premotor properties of saccadic versus cephalomotor circuits (Corneil and Munoz, 2014), as electrical stimulation frequencies Ͻϳ50 Hz are incapable of recruiting the brainstem saccadic burst generator (Tehovnik and Lee, 1993;Cavanaugh and Wurtz, 2004 …”

“…1B). These muscles contribute to horizontal head turns to the side of the muscle (Corneil et al, 2001) and are robustly recruited by extracellular stimulation of the FEF (Elsley et al, 2007) and the SEF (Chapman et al, 2012). Leads from these electrodes were tunneled subcutaneously up to the skull and connected to a connector embedded within the acrylic.…”

“…A series of results from our laboratory suggest that neck muscle activity provides an alternative, and perhaps a more sensitive, indicator of oculomotor activity (Corneil and Munoz, 2014). In NHPs, electrical microstimulation of the FEF evokes robust recruitment of a contralateral head-turning synergy (Elsley et al, 2007), which persists even if stimulation current is lower than that required to evoke saccades (Corneil et al, 2010).…”

“…In NHPs, electrical microstimulation of the FEF evokes robust recruitment of a contralateral head-turning synergy (Elsley et al, 2007), which persists even if stimulation current is lower than that required to evoke saccades (Corneil et al, 2010). Stimulation of the nearby supplementary eye fields (SEFs) evokes the same neck muscle response (Chapman et al, 2012), with the magni-tude of recruitment scaling with endogenous activity at the time of stimulation (Chapman and Corneil, 2014). Such state dependency is also a hallmark of TMS (for review, see Silvanto et al, 2008).…”

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

“…Notably, SC activity appears to represent the target abstractly, independent of whether the movement will be achieved by the eyes, head, body, or limbs. Indeed, this activity may even reflect the selection of a target to attend to, without any overt motor component at all (Carello and Krauzlis 2004;Corneil and Munoz 2014;Krauzlis et al 2013;Lovejoy and Krauzlis 2010). Instead, the specific combination of motor output required to achieve the goal of orienting to the target appears to be represented in the activity of brain stem premotor nuclei coordinated, in part, by the SC (Gandhi and Katnani 2011).…”