Neurons in the Primate Superior Colliculus Coding for Arm Movements in Gaze-Related Coordinates

Abstract

In the intermediate and deep layers of the superior colliculus (SC), a well-established oculomotor structure, a substantial population of cells is involved in the control of arm movements. To examine the reference frame of these neurons, we recorded in two rhesus monkeys (Macaca mulatta) the discharges of 331 neurons in the SC and the underlying mesencephalic reticular formation (MRF) while monkeys reached to the same target location during different gaze orientations. For 65 reach-related cells with sufficient data and for simultaneously recorded electromyograms (EMGs) of 11 arm muscles, we calculated an ANOVA (factors: target position, gaze angle) and a gaze-dependency (GD) index. EMGs and the activity of many (60%) of the reach-related neurons were not influenced by the target representation on the retina or eye position. We refer to these as "gaze-independent" reach neurons. For 40%, however, the GD fell outside the range of the muscle modulation, and the ANOVA showed a significant influence of gaze. These "gaze-related" reach neurons discharge only when the monkey reaches for targets having specific coordinates in relation to the gaze axis, i.e., for targets in a gaze-related "reach movement field" (RMF). Neuronal activity was not modulated by the specific path of the arm movement, the muscle pattern that is necessary for its realization or the arm that was used for the reach. In each SC we found gaze-related neurons with RMFs both in the contralateral and in the ipsilateral hemifield. The topographical organization of the gaze-related reach neurons in the SC could not be matched with the well-known visual and oculomotor maps. Gaze-related neurons were more modulated in their strength of activity with different directions of arm movements than were gaze-independent reach neurons. Gaze-related reach neurons were recorded at a median depth of 2.03 mm below SC surface in the intermediate layers, where they overlap with saccade-related burst neurons (median depth: 1.55 mm). Most of the gaze-independent reach cells were found in a median depth of 4.01 mm below the SC surface in the deep layers and in the underlying MRF. The gaze-related reach neurons operating in a gaze-centered coordinate system could signal either the desired target position with respect to gaze direction or the motor error between gaze axis and reach target. The gaze-independent reach neurons, possibly operating in a shoulder- or arm-centered reference frame, might carry signals closer to motor output. Together these two types of reach neurons add evidence to our hypothesis that the SC is involved in the sensorimotor transformation for eye-hand coordination in primates.

Looking for the GAP effect in manual responses and the role of contextual influences in reaction time experiments

“…Strong correlations between electromyographic activity of arm muscles and neuronal activity of a collicular "reach cell" have been found for proximal muscles. However, the correlation obtained for distal muscles, such as the flexor digitorum superficialis, was much less frequent and weak (18), confirming previous findings linking the superior colliculus to orienting movements of the eyes, head and arms (e.g., 17,21). So, if collicular mechanisms are, in fact, mediating the facilitation in the GAP paradigm, the GAP effect for key-press responses should be minimal or even nonexistent.…”

Inhibition of return in single and dual tasks: Examining saccadic, keypress, and pointing responses

“…Although Li and Lin (2002) and Kingstone and Pratt (1999) found more IOR for keypress-eye than for keypress-alone movements, this was not the case for the conjoined and independent pointing responses (hand and mouse) examined by Khatoon et al (2002). This separation on response types may occur because pointing responses require considerable SC involvement (Stuphorn, Bauswein, & Hoffmann, 2000;Werner, Dannenberg, & Hoffmann, 1997), with the inhibition in the SC essentially at ceiling and leaving little room for any additional inhibition associated with the saccade responses. Presumably, keypress responses-which have much lower spatial requirements and therefore require less SC activation-are well away from any maximal level of inhibition in the SC and are thus more likely to piggyback on saccadic IOR.…”

The relative timing between eye and hand in rapid sequential pointing is affected by time pressure, but not by advance knowledge

“…At a neural level, it has been suggested that timing between eyes and upper limb in pointing tasks relies on signal interchange and probably resides in the superior colliculus where signals of the oculomotor and manual control systems converge (Reyes-Puerta et al 2010;Stuphorn et al 2000;Werner et al 1997). Indeed, neuronal activity of the superior colliculus, an area classically linked with gaze fixation (Munoz and Wurtz 1993a, b), is known to be partly modulated by the arm movements involved in reaching (Reyes-Puerta et al 2010;Stuphorn et al 1999;Stuphorn et al 2000;Werner et al 1997).…”

“…Indeed, neuronal activity of the superior colliculus, an area classically linked with gaze fixation (Munoz and Wurtz 1993a, b), is known to be partly modulated by the arm movements involved in reaching (Reyes-Puerta et al 2010;Stuphorn et al 1999;Stuphorn et al 2000;Werner et al 1997). In this way, arm movement and the correlated 'reach neurons' can facilitate or inhibit gaze shifts by providing excitatory or inhibitory input to saccadic build-up neurons (Lünenburger et al 2000).…”