Role of the Primate Superior Colliculus in the Control of Head Movements

Abstract

One important behavioral role for head movements is to assist in the redirection of gaze. However, primates also frequently make head movements that do not involve changes in the line of sight. Virtually nothing is known about the neural basis of these head-only movements. In the present study, single-unit extracellular activity was recorded from the superior colliculus while monkeys performed behavioral tasks that permit the temporal dissociation of gaze shifts and head movements. We sought to determine whether superior colliculus contains neurons that modulate their activity in association with head movements in the absence of gaze shifts and whether classic gaze-related burst neurons also discharge for head-only movements. For 26% of the neurons in our sample, significant changes in average firing rate could be attributed to head-only movements. Most of these increased their firing rate immediately prior to the onset of a head movement and continued to discharge at elevated frequency until the offset of the movement. Others discharged at a tonic rate when the head was stable and decreased their activity, or paused, during head movements. For many putative head cells, average firing rate was found to be predictive of head displacement. Some neurons exhibited significant changes in activity associated with gaze, eye-only, and head-only movements, although none of the gaze-related burst neurons significantly modulated its activity in association with head-only movements. These results suggest the possibility that the superior colliculus plays a role in the control of head movements independent of gaze shifts.

Intrinsic Reference Frames of Superior Colliculus Visuomotor Receptive Fields during Head-Unrestrained Gaze Shifts

“…However, since some of our neurons preferred G over T, our data do not exclude the possibility that the SC is partially involved in the early computations for gaze kinematics (and see the next section on Gain modulation). Moreover, this study only examined gaze and did not address the question of whether some neurons have a preference for eye or head movement (Guitton, 1992;Freedman et al, 1996) (but see Walton et al, 2007Walton et al, , 2008. Finally, we could not distinguish the "visual burst" from the "motor burst" (Munoz and Wurtz, 1995;Walker et al, 1995), so it is possible that these two responses might show different results.…”

Firing Patterns in Superior Colliculus of Head-Unrestrained Monkey during Normal and Perturbed Gaze Saccades Reveal Short-Latency Feedback and a Sluggish Rostral Shift in Activity

“…Collicular head-movement related neurons (Walton et al, 2007) were unlikely involved because they are not the "gaze-related" cells studied here. The brake's click sound might have triggered a transient collicular response, but the ϳ10 ms response latency was much shorter than that previously described for SC responses to auditory stimuli (mean, 44.8 ms) (Jay and Sparks, 1987).…”

Target modality determines eye-head coordination in nonhuman primates: implications for gaze control

“…Hundreds of studies comprising numerous areas of the brain, e.g., the paramedian pontine reticular formation (Gandhi and Sparks 2007;Sparks et al 2002), the central mesencephalic reticular formation (Pathmanathan et al 2006a(Pathmanathan et al , 2006b, the pontomedullary region (Cowie and Robinson 1994;Cowie et al 1994), the inhibitory burst neuron area (Cullen and Guitton 1997), the nucleus raphe interpositus (Bergeron and Guitton 2002;Paré and Guitton 1990;Phillips et al 1999), the nucleus reticularis gigantocellularis (Freedman and Quessy 2004;Quessy and Freedman 2004), the caudal fastigial nucleus (Fuchs et al 2010;Quinet and Goffart 2005), the frontal eye fields (Bizzi and Schiller 1970;Chen 2006;Guitton andMandl 1978a, 1978b;Knight and Fuchs 2007;Tu and Keating 2000), the supplementary eye fields (Martinez-Trujillo et al 2003), and the SC (e.g., Corneil et al 2002aCorneil et al , 2002bFreedman and Sparks 1997a;Klier et al 2001;Munoz et al 1991;Rezvani and Corneil 2008;Walton et al 2007Walton et al , 2008, have been published on the subject. Although there is ample evidence that the eyes and head are moved by separate neural commands (Bizzi et al 1971;Corneil et al 2002b;Freedman and Sparks 2000), a persistent and most controversial question concerns the origin of those signals: Are they generated separately or are they decomposed from a gaze signal, and if so where?…”