Dissociation of reach-related and visual signals in the human superior colliculus
Introduction
Although the cortical networks subserving upper limb functions in humans are quite well understood, the contributions of deep brain structures to the control of our arms and hands remained elusive. Our knowledge about the role of brainstem structures in the sensorimotor systems is almost entirely based on animal models. The superior colliculus, located at the dorsal brainstem, is a structure with well-known functions in the context of oculomotor control and visual processing. It contains topographical maps of the visual, auditory and somatosensory world (Cynader and Berman, 1972, Jay and Sparks, 1987, Stein et al., 2002). Additionally, the results of a small number of neurophysiological reports suggested that neurons in the SC and the directly underlying mesencephalic reticular formation are active prior to and during a reaching movement executed with the contralateral arm (Lünenburger et al., 2001, Werner et al., 1997a, Werner et al., 1997b). Just recently, we reported reach-related signals in the human SC, exactly replicating previous findings in animals (Linzenbold and Himmelbach, 2012).
In our previous study (Linzenbold and Himmelbach, 2012) we identified reach-related signals in deep locations of the SC contralateral to the moving arm. We also observed similar signal increases in more dorsal, presumably superficial and intermediate locations of the respective contralateral SC. However, reach-related signals in these dorsal SC locations disappeared in a comparison of reaching with the control task, i.e. execution of reflexive saccades. This finding left us with two possible interpretations. Either, these dorsal reach-related signals were exclusively driven by the visual presentation of targets in both conditions (reaching and saccades) or these signals were, at least partially, driven by the execution of arm movements and the visual stimulation and saccade execution in the control task concealed this signal source. The latter possibility is supported by the anatomical distribution of reach-related neurons throughout the depth range of the primate SC (Werner et al., 1997a, Werner et al., 1997b). Therefore, we dissociated arm movement signals from visual signals in the present study. We separated the visual hemifields of target presentation in individual blocks (left targets vs. right targets) and instructed the participants to execute either direct movements to the presented targets (pro-reaching) or reach to a position opposite to the presented target (anti-reaching).
In agreement with our previous results, we found reliable BOLD signal increases during right arm reaching in dorsal and ventral locations of the left human SC in all conditions (Linzenbold and Himmelbach, 2012). Thus, signals in the left dorsal SC were also clearly above baseline if there was no contralateral visual stimulation. In contrast, in the right SC we found positive BOLD signals in the dorsal location only if there was contralateral visual stimulation.
Section snippets
Participants
Sixteen subjects (13 females, 3 males, mean age 28 years, range 23–35 years) participated in this experiment. All of them had normal or corrected-to-normal visual acuity. All participants gave their informed consent to participate in the study that was performed in accordance with the ethical standards established by the 1964 Declaration of Helsinki and approved by the local ethical committee.
Procedures
All measurements were conducted in complete darkness. We used a black, opaque film to cover all windows
Behavioural results
To ensure the reliability of the manual data analysis a randomly chosen subset of 27 hand movement videos was analysed by two research assistants independently from each other. We looked at the absolute time difference between movement onsets reported from both raters and found rare maximum deviations of 3 video frames. For most trials there was no difference between the raters at all or a difference of not more than a single frame. Thus, across 27 videos the mean absolute differences between
Discussion
In good agreement with our previous results we found reach related BOLD signal increases in the dorsal and ventral locations of the SC contralateral to the active arm. Beyond our previous work we showed that also signal changes in the contralateral dorsal locations were driven by the execution of arm movements irrespective of retinotopic target positions. In contrast, visual stimulation alone predicted signal increases only in the dorsal SC hemisphere contralateral to the stimulated hemifield.
Acknowledgments
This work was supported by the European Union (ERC StG 211078) and the Deutsche Forschungsgemeinschaft (HI 1371/1-1). We are grateful to Michael Erb and Uwe Klose from the Department of Neuroradiology for their technical support.
Conflict of interest statement
The authors have no conflict of interest to disclose.
References (24)
- et al.
Parietal modules for reaching
Neuropsychologia
(2009) - et al.
Spatiotopic organization in human superior colliculus observed with fMRI
Neuroimage
(2000) - et al.
Functional neuroimaging of the oculomotor brainstem network in humans
Neuroimage
(2011) - et al.
A possible role of the superior colliculus in eye–hand coordination
Prog. Brain Res.
(2001) - et al.
Functional imaging of the human superior colliculus: an optimised approach
Neuroimage
(2009) - et al.
Projections to the superior colliculus from inferior parietal, ventral premotor, and ventrolateral prefrontal areas involved in controlling goal-directed hand actions in the macaque
Cereb. Cortex
(2013) - et al.
Region of interest analysis using an SPM toolbox
Neuroimage
(2002) - et al.
Reaching to ipsilateral or contralateral targets: within-hemisphere visuomotor processing cannot explain hemispatial differences in motor control
Exp. Brain Res.
(1996) - et al.
Receptive-field organization of monkey superior colliculus
J. Neurophysiol.
(1972) - et al.
Role of primate superior colliculus in preparation and execution of anti-saccades and pro-saccades
J. Neurosci.
(1999)
Characteristics of “anti” saccades in man
Exp. Brain Res.
Anti-pointing is mediated by a perceptual bias of target location in left and right visual space
Exp. Brain Res.
Cited by (23)
Effect of dual tasking on a dynamic balance task in children with and without DCD
2021, Human Movement ScienceCitation Excerpt :A similar explanation was proposed in a study, where children with cerebral palsy were moving fast to moving targets and did not differ from controls (Smits-Engelsman, Rameckers, & Duysens, 2009). With respect to the underlying pathways, this may suggest that voluntary adjustments involve the prefrontal cortex (PFC), while fast automatic responses involve a faster pathway over the posterior parietal cortex (PPC) (Desmurget et al., 1999; Desmurget et al., 2001; Gréa et al., 2002; Pisella et al., 2000), or alternatively a subcortical path involving either the superior colliculi or the anterior cerebellum (Day & Brown, 2001; Desmurget et al., 2001; Gaveu et al., 2014; Himmelbach, Linzenbold, & Ilg, 2013; Linzenbold & Himmelbach, 2012; Liu, Ingram, Palace, & Miall, 1999). It is plausible that children with DCD use a different control strategy because they have more problems with divided attention (using cortical resources), are slower and more variable in their execution (Geuze, Jongmans, Schoemaker, & Smits-Engelsman, 2001; Mackenzie et al., 2008).
An innate brainstem self-other system involving orienting, affective responding, and polyvalent relational seeking: Some clinical implications for a “Deep Brain Reorienting” trauma psychotherapy approach
2020, Medical HypothesesCitation Excerpt :Here it will usually become clear if there are parallel sequences holding conflicting tendencies, for example, approach and defend urges occurring simultaneously and with different affective colouring, perhaps care/nurturing and fear. Reaching movements in attachment interactions have many cortical and subcortical substrates but the fundamental activation of these, especially when they are not tightly controlled through conscious awareness, is in the deep layers of the SC [108,109]. Shock and horror expressions, as are seen with some trauma memories, also occur before and after the affect comes into awareness and can be identified before emergence of the valenced SEEKING (S) state.
Polar-angle representation of saccadic eye movements in human superior colliculus
2018, NeuroImageCitation Excerpt :In humans, studies to infer SC function have historically been restricted to whole-brain functional magnetic resonance imaging (fMRI). Whole-brain or low-resolution (i.e., ≥2-mm voxels) fMRI has documented saccade-related activity in SC (de Weijer et al., 2010; Furlan et al., 2015; Krebs et al., 2010), and reach-related functions performed by the deep layers of SC (Himmelbach et al., 2013). However, the low-resolution measurements did not delineate the detailed topography of SC functions.
Response Inhibition
2015, Brain Mapping: An Encyclopedic Reference
- 1
Both authors contributed equally.