fMRI reveals a preference for near viewing in the human parieto-occipital cortex
Introduction
Human neuroimaging research has provided a wealth of findings that reflect how the visual world is spatially mapped in the cortex. This research, however, has focused mainly on the retinotopic organization of brain areas, primarily utilizing frontoparallel, two-dimensional stimuli. These techniques have shown that the left and right visual fields are represented in opposite hemispheres and that the upper and lower visual fields also have distinct cortical representations (e.g., Previc, 1990, Previc, 1998, Skrandies, 1987). Even finer spatial divisions can be observed with retinotopic mapping of occipital cortex (Grill-Spector and Malach, 2004). While these 2D spatial representations can tell us the direction of an object, they do little to tell us the distance of that object. This third dimension, depth, is a neglected area of neuroimaging research that is crucially important to understanding how we guide our actions.
Within the third dimension of depth, a critical distinction exists between peripersonal space, the region immediately surrounding the body that can be acted upon and the extrapersonal space that lies beyond it. This distinction has a long history (see Previc, 1998 and Marshall and Fink, 2001 for reviews) and has recently gained credence from a growing number of neuropsychological studies (Halligan and Marshall, 1991, Berti and Frassinetti, 2000, Vuilleumier et al., 1998, Longo and Lourenco, 2006, Bjoertomt et al., 2002).
The distinction between peripersonal and extrapersonal space is particularly important because only objects within peripersonal space can be acted upon by the body’s effectors, such as the arm, hand and head. Given that the dorsal visual stream (from occipital to posterior parietal cortex, PPC) plays a particularly important role in the visual guidance of actions (Goodale and Milner, 1992, Milner and Goodale, 1995), peripersonal space may be particularly relevant for cortical areas within the dorsal stream. Moreover, there are numerous regions within PPC that are specialized for guiding actions with a particular effector (see Andersen et al., 1997 for review), and each of these regions may be tuned to the optimal spatial range for that effector (see Iriki et al., 1996).
Other regions of the PPC may be specialized for the range of space around other body parts; in particular, within the fundus of the intraparietal sulcus (IPS) of the macaque, the ventral intraparietal (VIP) area appears to be specialized for near peripersonal space around the head and face. Electrophysiological studies conducted by Colby et al. (1993) found that VIP neurons responded to the presentation of moving objects and displayed higher activation when objects were moved near the face than when they were moved further away.
Given the similarities seen in visual areas across species, one might expect to find a similar region in the human PPC. A putative functional equivalent of macaque VIP (pVIP) has been proposed by Bremmer et al. (2001) who used fMRI to demonstrate polymodal (visual, tactile and auditory) responses in the human intraparietal sulcus (IPS). Preliminary results from our group (Goltz et al., 2001) also found responses in the same vicinity for looming objects. More recently, Sereno and Huang (2006) have reported that the area contains congruent visual and tactile maps for the space around the face similar to those seen in the macaque (Duhamel et al., 1998). These findings suggest that the human parietal cortex contains a region that shares some properties with macaque VIP. However, if this human region is truly a functional equivalent of macaque VIP, it should also display a clear preference for moving stimuli in near vs. far space.
We used functional magnetic resonance imaging (fMRI) to investigate whether any areas of the human brain, including pVIP and perhaps other areas within the dorsal stream, would show a stronger response for stimuli in peripersonal space than extrapersonal space. We began by identifying pVIP based on an independent localizer, which contrasted the response to a stimulus looming toward the face against a stationary stimulus (as in Goltz et al., 2001). We then investigated whether this area would demonstrate greater activation for stimuli moving near the head than stimuli moving at farther distances. This was achieved by presenting participants with a disk that moved toward and away from their faces at different distances: one distance was near the face, one distance was just within reach, and one distance was outside of reach. While we were interested in the response pattern in pVIP, we also performed voxelwise contrasts between near motion and far motion to determine whether any functional area(s) outside pVIP would also show a near-space preference. For example, we expected that areas involved in reaching and grasping (for recent reviews see Culham et al., 2006, Culham and Valyear, 2006) might also demonstrate a preference for stimuli within reach over those beyond reach.
To our surprise, the results of our first experiment revealed no reliable depth preference in pVIP; however, the voxelwise analyses found a region in the dorsal parieto-occipital sulcus (dPOS) that showed a robust and consistent gradient of activation (Near > Medium > Far) for moving, as well as stationary stimuli. In addition, we observed diffuse activation for near motion more generally within occipital cortex.
The preference we observed for stimuli in near-space could have arisen from several available cues to depth. Because our participants looked directly at the looming object, one strong cue to depth was the near response based on oculomotor cues. The near response occurs when subjects gaze at a close object, causing the eyes to rotate inward (convergence), the lens to thicken (accommodation), and the pupils to dilate. These three yoked responses – vergence, accommodation and pupillary diameter – are sometimes referred to as the near triad. In addition to these oculomotor cues, there were also differences in binocular disparity between the stimulus and the background at the three testing distances and these could have also provided a strong cue to depth. We conducted a second experiment to determine whether the near response alone was sufficient to drive the preference seen in dPOS and occipital cortex, in the absence of disparity and monocular cues. Participants simply verged their eyes to maintain fixation on a small spot of light at one of the three distances. In the absence of any other visual stimulation, we found a robust preference for near fixation over medium and far fixation in dPOS and other occipital regions.
Taken together, although we did not observe a near-space preference in the putative human equivalent of macaque VIP, it appears that humans do have a functional area that can reflect object distance based on oculomotor cues alone. As we will discuss, this region may form part of the dorsal stream and provide depth-related information to higher-tier areas involved in the visual control of actions.
Section snippets
Participants
Eight healthy adult volunteers (two males, six females, ages 23 through 28, mean age = 24.8 years) were recruited as participants and financially compensated. For all participants, visual acuity was normal or corrected-to-normal (with contact lenses) for the spatial ranges being tested. Participants had no known depth perception abnormalities and performed normally on tests of stereoscopic discrimination (with disparity thresholds of 40 arc sec or less on 3D Vectographs by Stereo Optical Co.,
Results: Experiment 1
The results of this experiment show that the region identified as pVIP, while showing clear motion selectivity, did not exhibit the near-space preference expected of a macaque VIP functional homologue. Voxelwise analyses on both individual and group data also failed to identify any parietal regions with a preference for near-space. However, we did identify a region at the dorsal end of the parieto-occipital sulcus (dPOS) that displayed a clear preference for objects in near-space, regardless of
Absence of a near-space preference in pVIP
We were surprised not to observe a near-space preference within putative VIP, either with a localizer-based or voxelwise approach. There are several possible explanations for the absence of the expected response based on the nature of the population response in fMRI, the methodology we employed and the challenges of proposing interspecies relationships regarding brain areas.
There may be difficulties in generalizing from the responses of single units in electrophysiology to the population
Experiment 2: near viewing preference—vergence eye position and accommodation
The results of Experiment 1 show that not only is dPOS capable of representing the distance of a moving object, similar to macaque VIP, but can also discriminate distance when objects remain stationary. Based on the results of our pilot experiment on three subjects, the near-space preference in dPOS is likely to be driven by the near response rather than by binocular disparity, monocular cues or object distance alone. To test this hypothesis more rigorously, we designed an experiment in which
Results: Experiment 2
We performed voxelwise contrasts both for individual subjects and for group averaged data in Talairach space. Both approaches show that area dPOS clearly demonstrates an activation gradient based on the oculomotor signals associated with fixating objects at different distances (Near > Medium > Far). In addition, a similar pattern was observed in more diffuse regions of occipital cortex.
Discussion: Experiment 2
The results of Experiment 2 clearly show that the oculomotor cues of the near response are sufficient to explain the near-space preference in dPOS seen in Experiment 1. Moreover, this increased activation during the near response is sustained over at least 16 s, likely reflecting a tonic distance-specific signal. Specifically, in the stable plateau of the time course, dPOS activation was significantly higher for the near fixation distance than for medium fixation, and likewise, activation in
General discussion
Given that one of the clearest brain regions demonstrating a preference for peripersonal space in the macaque monkey is area VIP, we set out to determine whether a proposed human functional equivalent would also display a near-space preference. We identified area pVIP in the human intraparietal sulcus based on a response to moving vs. stationary objects near the face. While our pVIP did display clear motion selectivity, it did not, however, display the near-space preference that one would
Acknowledgments
This study was funded by an Natural Sciences and Engineering Research Council of Canada operating grant and Ontario Premier’s Research Excellence Award to Jody Culham. We would also like to thank the following: James Danckert for use of his eye-tracking equipment; Haitao Yang for his assistance in collecting eye-tracking data; Dan Pulham and Jim Ladich for their assistance in building our testing equipment; Carol Colby for clarifications regarding her 1993 study; Patrizia Fattori, Claudio
References (120)
- et al.
Coordinate transformations in the representation of spatial information
Curr. Opin. Neurobiol.
(1993) - et al.
Two distinct neural effects of blinking on human visual processing
NeuroImage
(2005) - et al.
Human parietal cortex in action
Curr. Opin. Neurobiol.
(2006) - et al.
The role of parietal cortex in visuomotor control: what have we learned from neuroimaging?
Neuropsychologia
(2006) - et al.
Brain activation related to the representations of external space and body scheme in visuomotor control
NeuroImage
(2001) - et al.
Motion correction algorithms may create spurious brain activations in the absence of subject motion
NeuroImage
(2001) - et al.
Modulation of cell responses to horizontal disparities by ocular vergence in the visual cortex of the awake Macaca mulatta monkey
Neurosci. Letters
(1998) - et al.
Human cortical areas activated in relation to vergence eye movements—A PET study
NeuroImage
(1999) - et al.
Human cortical oscillations: a neuromagnetic view through the skull
Trends Neurosci.
(1997) - et al.
Adaptation: from single cells to BOLD signals
Trends Neurosci.
(2006)
On the nature of near space: effects of tool use and the transition to far space
Neuropsychologia
Parietal updating of limb posture: an event-related fMRI study
Neuropsychologia
Two cortical systems for reaching in central and peripheral vision
Neuron
The effect of gaze angle and fixation distance on the responses of neurons in V1, V2, and V4
Neuron
Encoding of spatial location by posterior parietal neurons
Science
Multimodal representation of space in the posterior parietal cortex and its use in planning movements
Annu. Rev. Neurosci.
Posterior parietal areas specialized for eye movements (LIP) and reach (PRR) using a common coordinate frame
Novartis Found. Symp.
Functional organization of human intraparietal and frontal cortex for attending, looking, and pointing
J. Neurosci.
Researchers misunderstand confidence intervals and standard error bars
Psychol. Methods
When far becomes near: remapping of space by tool use
J. Cogn. Neurosci.
Relations between individual differences in oculomotor resting states and visual inspection performance
Ergonomics
Spatial neglect in near and far space investigated by repetitive transcranial magnetic stimulation
Brain: J. Neurol.
Direction-selective motion blindness after unilateral posterior brain damage
Eur. J. Neurosci.
Contribution of retinal versus extraretinal signals towards visual localization in goal-directed movements
Exp. Brain Res.
Polymodal motion processing in posterior parietal and premotor cortex: a human fMRI study strongly implies equivalencies between humans and monkeys
Neuron
Activation in visual cortex correlates with the awareness of stereoscopic depth
J. Neurosci.
Event-related fMRI reveals a dissociation in the parietal lobe between transport and grip components in reach-to-grasp movements. Abstract submitted to the Society for Neuroscience
A common reference frame for movement plans in the posterior parietal cortex
Nat. Rev., Neurosci.
Ventral intraparietal area of the macaque: anatomic location and visual response properties
J. Neurophysiol.
FMRI evidence for a ‘parietal reach region’ in the human brain
Exp. Brain Res.
Functional neuroimaging: experimental design and analysis. Book chapter
Inference by eye: confidence intervals and how to read pictures of data
Am. Psychol.
Characterization of the human visual V6 complex by functional magnetic resonance imaging
Eur. J. Neurosci.
Eye position signal modulates a human parietal pointing region during memory-guided movements
J. Neurosci.
Eye position signals modulate early dorsal and ventral visual areas
Cereb. Cortex
Distance modulation of neural activity in the visual cortex
Science
Ventral intraparietal area of the macaque: congruent visual and somatic response properties
J. Neurophysiol.
A new anatomical landmark for reliable identification of human area V5/MT: a quantitative analysis of sulcal patterning
Cereb. Cortex
‘Arm-reaching’ neurons in the parietal area V6A of the macaque monkey
Eur. J. Neurosci.
Evidence for both reaching and grasping activity in the medial parieto-occipital cortex of the macaque
Eur. J. Neurosci.
Spatial tuning of reaching activity in the medial parieto-occipital cortex (area V6A) of macaque monkey
Eur. J. Neurosci.
Combination of hand and gaze signals during reaching: activity in parietal area 7 m of the monkey
J. Neurophysiol.
False cerebral activation on BOLD functional MR images: study of low-amplitude motion weakly correlated to stimulus
Am. J. Neuroradiol.
Stability of tonic vergence
Invest. Ophthalmol. Visual Sci.
Binocular distance perception
Psychol. Rev.
Eye position influence on the parieto-occipital area PO (V6) of the macaque monkey
Eur. J. Neurosci.
Functional demarcation of a border between areas V6 and V6A in the superior parietal gyrus of the macaque monkey
Eur. J. Neurosci.
Brain location and visual topography of cortical area V6A in the macaque monkey
Eur. J. Neurosci.
The cortical visual area V6: brain location and visual topography
Eur. J. Neurosci.
Cited by (114)
Functional organization of the caudal part of the human superior parietal lobule
2023, Neuroscience and Biobehavioral ReviewsThe macaque ventral intraparietal area has expanded into three homologue human parietal areas
2022, Progress in NeurobiologyVisuomotor control in the healthy and damaged brain
2021, Encyclopedia of Behavioral Neuroscience: Second EditionThe relationship between action, social and multisensory spaces
2023, Scientific Reports