The Locus of Motor Activity in the Superior Colliculus of the Rhesus Monkey Is Unaltered during Saccadic Adaptation

Abstract

The location of motor-related activity in the deeper layers of the superior colliculus (SC) is thought to generate a desired displacement command specifying the amplitude and direction of saccadic eye movements. However, the amplitude of saccadic eye movements made to visual targets can be systematically altered by surreptitiously moving the target location after the saccade has been initiated. Depending on whether the target is moved closer to or further from the fixation location, adaptation of saccade amplitude results in movements that are either smaller or larger than control movements. It remains an open question whether the SC specifies the desired movement to the original target location or whether SC activity specifies the vector of the amplitude-altered movement that is observed as adaptation progresses. We investigated this question by recording the activity of saccade-related burst neurons in the SC of head-restrained rhesus monkeys during both backward and forward saccadic adaptation. During adaptation in each direction, we find no evidence that is consistent with a change in the locus of SC activity despite changes in saccade amplitude; the location of SC motor-related activity does not appear to be remapped during either forward or backward saccadic adaptation. These data are inconsistent with hypotheses that propose a key role for the SC in mediating the changes in saccade amplitude observed during adaptation.

The lateral intraparietal area codes the location of saccade targets and not the dimension of the saccades that will be made to acquire them

“…It has been demonstrated that saccadic adaptation occurs at a point where the saccade is represented as a vector (Hopp and Fuchs 2006) and affects gaze before it is separated into its eye and head components (Cecala and Freedman 2009;Phillips et al 1997). Neurons in the superior colliculus, even neurons that do not have visual responses, represent target location and not saccade amplitude in both the head-fixed (Frens and Van Opstal 1997;Quessy et al 2010) and unrestrained (DeSouza et al 2011;Fernandez-Ruiz et al 2007) conditions. Electrical stimulation of the superior colliculus evokes the adapted saccade when the stimulation current is low, although at high current levels it evokes an unadapted saccade, perhaps because the stronger stimulation signal overwhelms the adaptation signal (Edelman and Goldberg 2002).…”

Adaptation and adaptation transfer characteristics of five different saccade types in the monkey

“…Indeed, when either targeting (Frens and Van Opstal 1997;cf. Takeichi et al 2007) or delayed (Quessy et al 2010) saccades undergo adaptation, the neuronal activity in the SC does not change, indicating that both targeting and delayed saccades use an adaptation site that is downstream of the SC. The short-latency express saccade is often considered to be a reactive saccade like a targeting saccade (for reviews see Hopp and Fuchs 2004;Pélisson et al 2010).…”

“…Takeichi et al 2007; delayed saccade : Quessy et al 2010). Neurophysiological studies during adaptation suggest that one downstream structure that likely participates in targeting saccade plasticity is the oculomotor vermis (OMV) of the cerebellum (Barash et al 1999;Catz et al 2005Catz et al , 2008Kojima et al 2010bKojima et al , 2011Soetedjo et al 2008;Soetedjo and Fuchs 2006;Takagi et al 1998).…”

Eye position effects in saccadic adaptation

“…Many detailed properties of the adaptation of different types of saccades in humans suggest that areas above or at the level of the SC are involved in saccadic adaptation (overview in Hopp and Fuchs 2004;Pelisson et al 2010). Physiological studies in monkeys, however, saw no evidence for adaptation in the collicular map (Edelman and Goldberg 2002;Frens and van Opstal 1997;Melis and van Gisbergen 1996;Quessy et al 2010) but only mild changes in the firing rates (Takeichi et al 2007). Retinotopic encoding of the saccade vector along with an eye position gain field is a common finding in much of the circuitry that generates a saccade [fastigial nucleus , NRTP (Crandall and Keller 1985), SC (Campos et al 2006;van Opstal et al 1995), LIP (Andersen et al 1990), and FEF (Cassanello and Ferrera 2007)].…”