The role of the ventral intraparietal area (VIP/pVIP) in parsing optic flow into visual motion caused by self-motion and visual motion produced by object-motion

Retinal image motion is a composite signal that contains information about two behaviourally significant factors: self-motion and the movement of environmental objects. It is thought that the brain separates the two relevant signals, and although multiple brain regions have been identified that respond selectively to the composite optic flow signal, which brain region(s) perform the parsing process remains unknown. Here, we present original evidence that the putative human ventral intraparietal area (pVIP), a region known to receive optic flow signals as well as independent self-motion signals from other sensory modalities, plays a critical role in the parsing process and acts to isolate object-motion. We localised pVIP using its multisensory response profile, and then tested its relative responses to simulated object-motion and self-motion stimuli; results indicated that responses were much stronger in pVIP to stimuli that specified object-motion. We report two further observations that will be significant for the future direction of research in this area; firstly, activation in pVIP was suppressed by distant stationary objects compared to the absence of objects or closer objects. Secondly, we describe several other brain regions that share with pVIP selectivity for visual object-motion over visual self-motion as well as a multisensory response

Rapid enhancement of touch from non-informative vision of the hand

Processing in one sensory modality may modulate processing in another. Here we investigate how simply viewing the hand can influence the sense of touch. Previous studies showed that non-informative vision of the hand enhances tactile acuity, relative to viewing an object at the same location. However, it remains unclear whether this Visual Enhancement of Touch (VET) involves a phasic enhancement of tactile processing circuits triggered by the visual event of seeing the hand, or more prolonged, tonic neuroplastic changes, such as recruitment of additional cortical areas for tactile processing. We recorded somatosensory evoked potentials (SEPs) evoked by electrical stimulation of the right middle finger, both before and shortly after viewing either the right hand, or a neutral object presented via a mirror. Crucially, and unlike prior studies, our visual exposures were unpredictable and brief, in addition to being non-informative about touch. Viewing the hand, as opposed to viewing an object, enhanced tactile spatial discrimination measured using grating orientation judgements, and also the P50 SEP component, which has been linked to early somatosensory cortical processing. This was a trial-specific, phasic effect, occurring within a few seconds of each visual onset, rather than an accumulating, tonic effect. Thus, somatosensory cortical modulation can be triggered even by a brief, non-informative glimpse of one’s hand. Such rapid multisensory modulation reveals novel aspects of the specialised brain systems for functionally representing the body

Multisensory Integration in Self Motion Perception

Self motion perception involves the integration of visual, vestibular, somatosensory and motor signals. This article reviews the findings from single unit electrophysiology, functional and structural magnetic resonance imaging and psychophysics to present an update on how the human and non-human primate brain integrates multisensory information to estimate one's position and motion in space. The results indicate that there is a network of regions in the non-human primate and human brain that processes self motion cues from the different sense modalities

Neurophysiology of the macaque fronto-parietal magnitude system

In primates, the magnitude system resides in a fronto-parietal network. Single neurons in the monkey prefrontal cortex (PFC) and ventral intraparietal area (VIP) exhibit higher responses to a certain number of stimulus items regardless of their appearance or even sensory modality. Neuroimaging studies in humans show corresponding activation in human fronto-parietal areas during enumeration tasks. However, these areas are also involved in many other executive functions and, thus, the responses of single neurons within the network could be shaped by many factors. Understanding how information about magnitude develops within single neurons in this network was the objective of this thesis. This thesis includes five studies addressing various aspects of the primate frontoparietal magnitude system. First, we determined the role of behavioural relevance in shaping neuronal responses to number. Using enumerable coloured stimuli that naïve macaque monkeys discriminated based on their colour rather than number, we examined the selectivity of neuronal responses towards the number of stimuli. We simultaneously recorded single neurons in VIP and PFC. We compared these neurons to those recorded after a period of training for both monkeys, while they discriminated the stimuli based on number. In all the recording sessions, we also mapped the visual receptive fields (RF) of neurons using a passive fixation task. We created RF maps for a large number of spatially-selective neurons in each area and compared the RFs of pairs of neurons recorded at the same electrode tip. We then differentiated the extent of interaction between the RF and number selectivity in both areas. Neurons in both PFC and VIP were selective for number despite the monkeys being numerically-naïve and number being the behaviourally irrelevant stimulus feature. Post training, neurons in PFC were modulated by behavioural relevance and their selectivity for number became stronger as a result. VIP neurons did not show such an effect. We found that PFC RFs were predominantly contralateral and VIP RFs, foveal. Regardless of RF location and size, we observed heterogeneous and sometimes, inverted RFs in neurons adjacent to each other, more frequently in PFC than in VIP. Lastly, neurons in both PFC and VIP were strongly number-selective even when the number stimuli were shown outside their RFs. Our results provided valuable insight into the organisation of the magnitude system in primates. The presence of number-selective neuronal responses in numerically-naïve monkeys even when the number of stimuli was behaviourally irrelevant confirmed that our magnitude system processes magnitude spontaneously as a natural category. The strict spatiotopic organisation of RFs characteristic of early visual areas is progressively lower in VIP and PFC. Together, these results point to a hierarchy in the fronto-parietal areas we studied, with PFC located at the apex of the magnitude system and VIP upstream to it

Interaction of cortical networks mediating object motion detection by moving observers

Published in final edited form as: Exp Brain Res. 2012 August ; 221(2): 177–189. doi:10.1007/s00221-012-3159-8.The task of parceling perceived visual motion into self- and object motion components is critical to safe and accurate visually guided navigation. In this paper, we used functional magnetic resonance imaging to determine the cortical areas functionally active in this task and the pattern connectivity among them to investigate the cortical regions of interest and networks that allow subjects to detect object motion separately from induced self-motion. Subjects were presented with nine textured objects during simulated forward self-motion and were asked to identify the target object, which had an additional, independent motion component toward or away from the observer. Cortical activation was distributed among occipital, intra-parietal and fronto-parietal areas. We performed a network analysis of connectivity data derived from partial correlation and multivariate Granger causality analyses among functionally active areas. This revealed four coarsely separated network clusters: bilateral V1 and V2; visually responsive occipito-temporal areas, including bilateral LO, V3A, KO (V3B) and hMT; bilateral VIP, DIPSM and right precuneus; and a cluster of higher, primarily left hemispheric regions, including the central sulcus, post-, pre- and sub-central sulci, pre-central gyrus, and FEF. We suggest that the visually responsive networks are involved in forming the representation of the visual stimulus, while the higher, left hemisphere cluster is involved in mediating the interpretation of the stimulus for action. Our main focus was on the relationships of activations during our task among the visually responsive areas. To determine the properties of the mechanism corresponding to the visual processing networks, we compared subjects’ psychophysical performance to a model of object motion detection based solely on relative motion among objects and found that it was inconsistent with observer performance. Our results support the use of scene context (e.g., eccentricity, depth) in the detection of object motion. We suggest that the cortical activation and visually responsive networks provide a potential substrate for this computation.This work was supported by NIH grant RO1NS064100 to L.M.V. We thank Victor Solo for discussions regarding models of functional connectivity and our subjects for participating in the psychophysical and fMRI experiments. This research was carried out in part at the Athinoula A. Martinos Center for Biomedical Imaging at the Massachusetts General Hospital, using resources provided by the Center for Functional Neuroimaging Technologies, P41RR14075, a P41 Regional Resource supported by the Biomedical Technology Program of the National Center for Research Resources (NCRR), National Institutes of Health. This work also involved the use of instrumentation supported by the NCRR Shared Instrumentation Grant Program and/or High-End Instrumentation Grant Program; specifically, grant number S10RR021110. (RO1NS064100 - NIH; National Center for Research Resources (NCRR), National Institutes of Health; S10RR021110 - NCRR)Accepted manuscrip

Distributed Representation of Curvilinear Self-Motion in the Macaque Parietal Cortex

SummaryInformation about translations and rotations of the body is critical for complex self-motion perception during spatial navigation. However, little is known about the nature and function of their convergence in the cortex. We measured neural activity in multiple areas in the macaque parietal cortex in response to three different types of body motion applied through a motion platform: translation, rotation, and combined stimuli, i.e., curvilinear motion. We found a continuous representation of motion types in each area. In contrast to single-modality cells preferring either translation-only or rotation-only stimuli, convergent cells tend to be optimally tuned to curvilinear motion. A weighted summation model captured the data well, suggesting that translation and rotation signals are integrated subadditively in the cortex. Interestingly, variation in the activity of convergent cells parallels behavioral outputs reported in human psychophysical experiments. We conclude that representation of curvilinear self-motion perception is widely distributed in the primate sensory cortex

Linking pain and the body: neural correlates of visually induced analgesia

The visual context of seeing the body can reduce the experience of acute pain, producing a multisensory analgesia. Here we investigated the neural correlates of this “visually induced analgesia” using fMRI. We induced acute pain with an infrared laser while human participants looked either at their stimulated right hand or at another object. Behavioral results confirmed the expected analgesic effect of seeing the body, while fMRI results revealed an associated reduction of laser-induced activity in ipsilateral primary somatosensory cortex (SI) and contralateral operculoinsular cortex during the visual context of seeing the body. We further identified two known cortical networks activated by sensory stimulation: (1) a set of brain areas consistently activated by painful stimuli (the so-called “pain matrix”), and (2) an extensive set of posterior brain areas activated by the visual perception of the body (“visual body network”). Connectivity analyses via psychophysiological interactions revealed that the visual context of seeing the body increased effective connectivity (i.e., functional coupling) between posterior parietal nodes of the visual body network and the purported pain matrix. Increased connectivity with these posterior parietal nodes was seen for several pain-related regions, including somatosensory area SII, anterior and posterior insula, and anterior cingulate cortex. These findings suggest that visually induced analgesia does not involve an overall reduction of the cortical response elicited by laser stimulation, but is consequent to the interplay between the brain's pain network and a posterior network for body perception, resulting in modulation of the experience of pain

More than skin deep: body representation beyond primary somatosensory cortex

The neural circuits underlying initial sensory processing of somatic information are relatively well understood. In contrast, the processes that go beyond primary somatosensation to create more abstract representations related to the body are less clear. In this review, we focus on two classes of higher-order processing beyond somatosensation. Somatoperception refers to the process of perceiving the body itself, and particularly of ensuring somatic perceptual constancy. We review three key elements of somatoperception: (a) remapping information from the body surface into an egocentric reference frame (b) exteroceptive perception of objects in the external world through their contact with the body and (c) interoceptive percepts about the nature and state of the body itself. Somatorepresentation, in contrast, refers to the essentially cognitive process of constructing semantic knowledge and attitudes about the body, including: (d) lexical-semantic knowledge about bodies generally and one’s own body specifically, (e) configural knowledge about the structure of bodies, (f) emotions and attitudes directed towards one’s own body, and (g) the link between physical body and psychological self. We review a wide range of neuropsychological, neuroimaging and neurophysiological data to explore the dissociation between these different aspects of higher somatosensory function