Research reportVisual processing of optic flow and motor control in the human posterior cingulate sulcus
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.
References (30)
- et al.
Tonotopic organization of the human auditory cortex as detected by BOLD-FMRI
Hearing Research
(1998) - et al.
Improved optimization for the robust and accurate linear registration and motion correction of brain images
NeuroImage
(2002) - et al.
A global optimisation method for robust affine registration of brain images
Medical Image Analysis
(2001) - et al.
Forward models for physiological motor control
Neural Networks
(1996) - et al.
The representation of egomotion in the human brain
Current Biology
(2008) - et al.
Temporal autocorrelation in univariate linear modeling of FMRI data
NeuroImage
(2001) - et al.
Neuroimaging evidence of the anatomo-functional organization of the human cingulate motor areas
Cerebral Cortex
(2012) - et al.
Non-linear registration, aka Spatial normalisation
(2007) - et al.
Non-linear optimisation
(2007) - et al.
The posterior cingulate cortex and planum temporale/parietal operculum are activated by coherent visual motion
Visual Neuroscience
(2008)
Multi-subject null hypothesis testing using a fully bayesian framework: theory
An fMRI study of parietal cortex involvement in the visual guidance of locomotion
Journal of Experimental Psychology: Human Perception and Performance
Central cancellation of self-produced tickle sensation
Nature Neuroscience
Sensitivity of human visual cortical area V6 to stereoscopic depth gradients associated with self-motion
Journal of Neurophysiology
Optic flow and heading judgments [abstract]
Investigative Ophthalmology & Visual Science
Cited by (16)
Preference for locomotion-compatible curved paths and forward direction of self-motion in somatomotor and visual areas
2021, CortexCitation Excerpt :This is in good agreement with the fact that V6+ is an early extrastriate motion-sensitive visual area (Pitzalis et al., 2010, 2013a) which is retinotopically organized (Pitzalis et al., 2006) and is able to discriminate among different types of self-motion (i.e., translational, circular, radial and spiral motion, Pitzalis, Sdoia, et al., 2013). Also egomotion visual areas CSv and pCi (Antal et al., 2008; Cardin & Smith, 2010; Field et al., 2015; Fischer et al., 2012; Furlan et al., 2014; Pitzalis et al., 2020; Serra et al., 2019; Uesaki & Ashida, 2015; Wada et al., 2016; Wall & Smith, 2008) are good candidates for the analysis of self-motion aspects with different functional meanings. For example, CSv is a multisensory region receiving also vestibular input (Smith et al., 2012, 2017, 2018; Greenlee et al., 2016), indicating that this area participates in processing multimodal signals associated with whole-body motion.
What cortical areas are responsible for blindsight in hemianopic patients?
2020, CortexCitation Excerpt :Both areas are considered to be crucial hubs of the Default Mode Network (DMN) and are structurally and functionally connected to the mesial prefrontal and inferior parietal cortex, see Khalsa, Mayhew, Chechlacz, Bagary, and Bagshaw (2014); Wang, Chang, Chuang, and Liu (2019) and this raises intriguing questions about the role of this network in cognition and in awareness (see Leech & Sharp, 2014). However, a more specific reason for relating the Posterior Cingulate Gyrus to our behavioral and perceptual results is that it contains a visual processing area selective for optic flow that lies in the fundus of the cingulate sulcus (Field, Inman, & Li, 2015) and that is activated by coherent visual motion (Antal, Baudewig, Paulus, & Dechent, 2008). Thus, this area that is practically spared in Group 2 patients might explain the presence of an above-chance discrimination of moving versus stationary gratings as well as contribute to reports of perceptual awareness given that a moving grating is probably more salient than a static one (see Phillips, 2019).
The role of the ventral intraparietal area (VIP/pVIP) in the perception of object-motion and self-motion
2020, NeuroImageCitation Excerpt :During the baseline blocks static dots replaced optic flow. With the exception of the use of the BOLDscreen visual display, the stimulus was identical to that used in the investigation of CIngulate Sulcus Visual area by Field et al., 2015, where full technical details are provided. The sensation of tactile motion was produced by propelling room air across the participants face from a tube fixed to the head coil.
Children with developmental coordination disorder show altered functional connectivity compared to peers
2020, NeuroImage: ClinicalCitation Excerpt :The PCC [Brodmann area (BA) 23 and 31] and the precuneus (BA 7 and 31) are components of several functional networks, including the default mode network, dorsal attention network, and fronto-parietal networks (Leech and Sharp, 2014; Cavanna and Trimble, 2006). The PCC is involved in many cognitive functions, including visual processing (Field et al., 2015; Hinkley et al., 2009), visuospatial navigation (Bzdok et al., 2015), decision-making (Heilbronner et al., 2011), working memory involving images (Baker et al., 2018), memory retrieval and emotion processing (Bzdok et al., 2015; Baker et al., 2018), and in motor performance (Field et al., 2015; Amiez and Petrides, 2014). The precuneus is active in self-related processes, such as during autobiographical (Addis et al., 2004) and episodic memory retrieval (Vilberg and Rugg, 2008; Dörfel et al., 2009), and during visuospatial processing (Cavanna and Trimble, 2006; Schott et al., 2019; Byrne et al., 2007; Brodt et al., 2016), navigation (Brodt et al., 2016), and motor imagery (Hétu et al., 2013).
Neural sensitivity to translational self- and object-motion velocities
2024, Human Brain Mapping
- 1
Tel.: +44 118 3785004.