Elsevier

NeuroImage

Volume 82, 15 November 2013, Pages 61-67
NeuroImage

Dissociation of reach-related and visual signals in the human superior colliculus

https://doi.org/10.1016/j.neuroimage.2013.05.101Get rights and content

Highlights

  • We measured fMRI BOLD-responses during anti- and pro-reaching in humans.

  • We analysed signals in selected regions-of-interest in the superior colliculus.

  • We distinguished between visual and reach-related signals.

  • Ventral positions of the SC revealed reach signals contralateral to the active arm.

  • Dorsal positions of the SC showed visual and reach-related signals.

Abstract

Electrophysiological and micro-stimulation studies in non-human animal species indicated that the superior colliculus (SC) plays a role in the control of upper limb movements. In our previous work we found reach-related signals in the deep superior colliculus in humans. Here we show that also signals in more dorsal locations are correlated with the execution of arm movements. We instructed healthy participants to reach for visual targets either presented in the left or in the right visual hemifield during an fMRI measurement. Visual stimulation was dissociated from movement execution using a pro- and anti-reaching task. Thereby, we successfully differentiated between signals at these locations induced by the visual input of target presentations on the one hand and by the execution of arm movements on the other hand. Extending our previous report, the results of this study are in good agreement with the observed anatomical distribution of reach-related neurons in macaques. Obviously, reach-related signals can be found across a considerable depth range also in humans.

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)

  • B. Fischer et al.

    Characteristics of “anti” saccades in man

    Exp. Brain Res.

    (1992)
  • M. Heath et al.

    Anti-pointing is mediated by a perceptual bias of target location in left and right visual space

    Exp. Brain Res.

    (2009)
  • Cited by (0)

    1

    Both authors contributed equally.

    View full text