Elsevier

Cortex

Volume 71, October 2015, Pages 377-389
Cortex

Research report
Visual processing of optic flow and motor control in the human posterior cingulate sulcus

https://doi.org/10.1016/j.cortex.2015.07.014Get rights and content

Abstract

Previous studies have shown that the human posterior cingulate contains a visual processing area selective for optic flow (CSv). However, other studies performed in both humans and monkeys have identified a somatotopic motor region at the same location (CMA). Taken together, these findings suggested the possibility that the posterior cingulate contains a single visuomotor integration region. To test this idea we used fMRI to identify both visual and motor areas of the posterior cingulate in the same brains and to test the activity of those regions during a visuomotor task. Results indicated that rather than a single visuomotor region the posterior cingulate contains adjacent but separate motor and visual regions. CSv lies in the fundus of the cingulate sulcus, while CMA lies in the dorsal bank of the sulcus, slightly superior in terms of stereotaxic coordinates. A surprising and novel finding was that activity in CSv was suppressed during the visuomotor task, despite the visual stimulus being identical to that used to localize the region. This may provide an important clue to the specific role played by this region in the utilization of optic flow to control self-motion.

Introduction

Control of self-motion is of fundamental importance. Self-motion generates a specific type of visual information referred to as optic flow, and many studies have sought to identify the cortical network and neural mechanisms associated with the processing of this information. Previous studies of the human posterior cingulate sulcus have revealed that a key part of the network is a bilateral visually responsive region, named cingulate sulcus visual area (CSv), specialised for the processing of optic flow (e.g., Furlan et al., 2013, Wall and Smith, 2008). This region responds bilaterally even when visual flow is confined to one visual field (Fischer, Bülthoff, Logothetis, & Bartels, 2012). CSv also receives vestibular input (Cardin and Smith, 2011, Smith et al., 2012), which is clearly consistent with the proposal that it has a role in the perception and control of self-motion. However, CSv has not been identified in monkeys. Instead, previous studies have identified three motor areas that show somatotopic organization in the banks of the cingulate sulcus of monkeys: a rostral cingulate motor area (CMA) lies inferior to the pre-supplementary motor area, and two caudal CMA's are found ventral to the supplementary motor area – one in the dorsal bank of the cingulate and one on the ventral bank (Amiez and Petrides, 2012, Picard and Strick, 1996). The human homologs of the two caudal CMA's are located close to the reported location of CSv as localised with visual stimuli. For example, Fischer et al. (2012) report the MNI coordinates of CSv at X = −13 ± 3, Y = −26 ± 5, Z = 42 ± 3 in the left hemisphere and X = 13 ± 3, Y = −26 ± 8, Z = 45 ± 3 in the right hemisphere. This may be compared with Picard and Strick's coordinates for ‘posterior hand movement region 2’ (one of the two human homologues of monkey caudal CMA) at ±X = 7.4 ± 4.2, Y = −29.4 ± 5.8, Z = 48 ± 5.4 for participants whose anatomy lacked the paracingulate sulcus at the location of activation and ±X = 8.9 ± 4.4, Y = −33.4 ± 11, Z = 47.1 ± 7.1 for those whose anatomy did include the paracingulate sulcus. The general location of these visual and motor regions is shown in Fig. 1.

Due to the variability of mean coordinates reported for CSv between studies [e.g., the MNI coordinates for CSv given by Pitzalis et al. (2013) are ±X = 15, Y = −33, Z = 39, Antal, Baudewig, Paulus, and Dechent (2008) give X = −12, Y = −24, Z = 39 and X = 10, Y = −28, Z = 42, while Fischer et al. (2012) give X = −13 ± 3, Y = −26 ± 5, Z = 42 ± 3 and X = 13 ± 3, Y = −26 ± 8, Z = 45 ± 3], it is difficult to compare CSv activations with caudal CMA activations. For example, the reported posterior–anterior location of CSv is sufficiently variable to place it either posterior or anterior to reported caudal CMA coordinates. Existing studies have either used optic flow stimuli aimed at probing the properties of CSv, or simple motor tasks aimed at probing the properties of CMA, but to our knowledge no study has used both types of task as localisers in the same participants. Given this and the spatial resolution of fMRI group results, it still remains in question whether the reported CSv and CMA in the posterior cingulate are two adjacent but separate regions, or a single 'visuomotor' integration region containing both motor neurons and optic flow tuned neurons that interact, or motor neurons that also possess optic flow receptive fields.

The current study is designed to address the above question. Specifically, we used a motor, a visual, and an integrated visuomotor task to localize and differentiate CMA and CSv in the posterior cingulate sulcus in humans. In the motor task participants moved a joystick in response to a tone, and in the visual task they fixated centrally while viewing a changing optic flow field. The visuomotor task used the same visual conditions as the visual task but in addition the participants moved a joystick to track the path trajectory of forward self-motion within the flow field. If CMA and CSv are two separate regions, we would expect to observe contralateral activation in the posterior cingulate for the pure motor task, and bilateral activation that does not overlap with the motor activation for the pure visual task. In the case of the integrated visuomotor task in which optic flow is used to control the parameters of a motor response, activation should occur bilaterally and be the sum of pure visual and pure motor activations. In contrast, if CSv/CMA is a single integration region, we would expect to observe that the pure visual task produces bilateral activation and that the pure motor task produces a contralateral activation that considerably overlaps the visual activation. Under this hypothesis the visuomotor task should produce the same bilateral pattern of activation as the pure visual task.

Section snippets

Participants

The study had 17 participants (5 male, age range 19–46, mean 24 years), who gave their informed written consent prior to taking part. The study was approved by the University of Reading Research Ethics Committee. Nine participants performed the motor and the visuomotor tasks right-handed, and eight left-handed. All participants performed the visual task.

Tasks and stimuli

Three tasks were used in the current study. The motor task was based on that used by Deiber et al. (1991) to localize CMA. The task had two

Localization of CSv and CMA

The visual task that involved passive viewing of optic flow produced a bilateral activation in the posterior cingulate compared with fixation of a static flow field. To confirm that the activation was specific to optic flow rather than simply related to visual stimulation we performed a group average analysis subtracting the scrambled flow condition from the optic flow condition. Bilateral activation survived the contrast (Fig. 2), replicating previous findings and confirming that we were

Discussion

We found that CMA and CSv are separate functional brain regions that are close neighbours in stereotaxic space. However, considering the grey matter as a folded sheet the two areas have very distinct locations – CSv is located in the fundus of the cingulate sulcus and CMA lies on the dorsal bank of the sulcus and extends further towards the medial surface as well as being much more extensive than CSv in the anterior–posterior dimension. The possibility that CMA and CSv together comprise a

Acknowledgements

This study was supported by a grant from the Research Grants Council of Hong Kong (<http://rcgas.hku.hk/Project/PrjDetail.aspx?prj_code=103487>HKU>748010H) to L. Li and D. T. Field. We thank two anonymous reviewers for their comments on a previous draft of the manuscript.

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