Influence of Task Predictability on the Activity of Neurons in the Rostral Superior Colliculus During Double-Step Saccades

Abstract

Target probability has been shown to modulate motor preparatory activity of neurons in the caudal superior colliculus (SC) of the primate. Here we tested whether top-down processes, such as task predictability, influence the activity of neurons also at the rostral pole of the SC (rSC), classically related to fixation. To investigate this, double-step saccade tasks were embedded in two different paradigms, one containing unpredictable and another containing predictable tasks. During predictable tasks the animals could develop some expectation about the forthcoming second target jump, i.e., anticipate when and where to make the second saccade. Neuronal responses were recorded during both paradigms and compared, revealing the influence of task predictability on the activity of rSC neurons during specific periods of fixation. In particular, neuronal activity stayed significantly lower during the fixation period between two successive saccades in predictable than in unpredictable tasks. In addition there was a learning effect within a session during predictable conditions, i.e., the intersaccadic activity was higher in the early than in the late trials. Further, reaction times for the second saccade were shorter in predictable than in unpredictable tasks. However, we demonstrated that this difference in reaction times cannot be solely accounted for by the reported difference in neural activity, which was mainly influenced by the predictability of the tasks. With these results we show that top-down processes such as predictability are imposed on the activity of neurons in the rostral pole of the primate SC.

Neuronal activity in the superior colliculus related to saccade initiation during coordinated gaze–reach movements

“…Indeed, similar top‐down cognitive signals have been reported in the activity of rSC neurons by means of the pro‐/anti‐saccade paradigm (Everling et al. , 1999) and predictable/unpredictable double‐step saccades (Reyes‐Puerta et al. , 2009).…”

“…Third, previous studies have shown that the activity of rSC neurons is task dependent, even when the visual stimuli used in the different tasks are identical – and therefore not presenting trivial visual effects (Everling et al. , 1999; Reyes‐Puerta et al. , 2009).…”

“…Significant differences have been previously reported in the activity of rSC neurons through the manipulation of top‐down cognitive signals by means of the pro‐/anti‐saccade paradigm (Everling et al. , 1999) and predictable/unpredictable double‐step saccades (Reyes‐Puerta et al. , 2009).…”

“…, 1997), the pro‐/anti‐saccade paradigm (Everling et al. , 1999), and by manipulating task predictability during double‐step saccades (Reyes‐Puerta et al. , 2009).…”

The efference cascade, consciousness, and its self: naturalizing the first person pivot of action control

“…This provides a rationale for non-sensory collicular afference such as that originating in cortical association areas and hypothalamus, and more generally the conspicuous convergence of exogenous (bottom-up) and endogenous (top-down) information sources in the superior colliculus (cf. Lines and Milner, 1985; Rieck et al, 1986; Cooper et al, 1998; Trappenberg et al, 2001; Felsen and Mainen, 2008; Reyes-Puerta et al, 2009; Cohen and Castro-Alamancos, 2010; Meeter et al, 2010; Maior et al, 2012). …”