The macaque ventral intraparietal area has expanded into three homologue human parietal areas

Macaque ventral intraparietal area (VIP) in the fundus of the intraparietal sulcus has been implicated in a diverse range of sensorimotor and cognitive functions such as motion processing, multisensory integration, processing of head peripersonal space, defensive behavior, and numerosity coding. Here, we exhaustively review macaque VIP function, cytoarchitectonics, and anatomical connectivity and integrate it with human studies that have attempted to identify a potential human VIP homologue. We show that human VIP research has consistently identified three, rather than one, bilateral parietal areas that each appear to subsume some, but not all, of the macaque area’s functionality. Available evidence suggests that this human “VIP complex” has evolved as an expansion of the macaque area, but that some precursory specialization within macaque VIP has been previously overlooked. The three human areas are dominated, roughly, by coding the head or self in the environment, visual heading direction, and the peripersonal environment around the head, respectively. A unifying functional principle may be best described as prediction in space and time, linking VIP to state estimation as a key parietal sensorimotor function. VIP’s expansive differentiation of head and self-related processing may have been key in the emergence of human bodily self-consciousness.

Action-dependent processing of self-motion in parietal cortex of macaque monkeys

Successful interaction with the environment requires the dissociation of self-induced from externally induced sensory stimulation. Temporal proximity of action and effect is hereby often used as an indicator of whether an observed event should be interpreted as a result of own actions or not. We tested how the delay between an action (press of a touch bar) and an effect (onset of simulated self-motion) influences the processing of visually simulated self-motion in the ventral intraparietal area (VIP) of macaque monkeys. We found that a delay between the action and the start of the self-motion stimulus led to a rise of activity above the baseline activity before motion onset in a subpopulation of 21% of the investigated neurons. In the responses to the stimulus, we found a significantly lower sustained activity when the press of a touch bar and the motion onset were contiguous compared to the condition when the motion onset was delayed. We speculate that this weak inhibitory effect might be part of a mechanism that sharpens the tuning of VIP neurons during self-induced motion and thus has the potential to increase the precision of heading information that is required to adjust the orientation of self-motion in everyday navigational tasks.

Spatial Neuronal Integration Supports a Global Representation of Visual Numerosity in Primate Association Cortices

Our sense of number rests on the activity of neurons that are tuned to the number of items and show great invariance across display formats and modalities. Whether numerosity coding becomes abstracted from local spatial representations characteristic of visual input is not known. We mapped the visual receptive fields (RFs) of numerosity-selective neurons in the pFC and ventral intraparietal area in rhesus monkeys. We found numerosity selectivity in pFC and ventral intraparietal neurons irrespective of whether they exhibited an RF and independent of the location of their RFs. RFs were not predictive of the preference of numerosity-selective neurons. Furthermore, the presence and location of RFs had no impact on tuning width and quality of the numerosity-selective neurons. These findings show that neurons in frontal and parietal cortices integrate abstract visuospatial stimuli to give rise to global and spatially released number representations as required for number perception.

Mapping numerical perception and operations in relation to functional and anatomical landmarks of human parietal cortex

Human functional imaging has identified the middle part of the intraparietal sulcus (IPS) as an important brain substrate for different types of numerical tasks. This area is often equated with the macaque ventral intraparietal area (VIP) where neuronal selectivity for non-symbolic numbers is found. However, the low spatial resolution and whole-brain averaging analysis performed in most fMRI studies limit the extent to which an exact correspondence of activation in different numerical tasks with specific sub-regions of the IPS can be established. Here we disentangled the functional neuroanatomy of numerical perception and operations (comparison and calculation) by acquiring high-resolution 7T fMRI data in a group of human adults, and relating the activations in different numerical contrasts to anatomical and functional landmarks on the cortical surface. Our results reveal a functional heterogeneity within human intraparietal cortex where the visual field map representations in superior/medial parts of IPS and superior parietal gyrus are involved predominantly in numerosity perception, whereas numerical operations predominantly recruit lateral/inferior parts of IPS. Since calculation and comparison-related activity fell mainly outside the field map representations considered the functional equivalent of the monkey VIP/LIP complex, the areas most activated during such numerical operations in humans are likely different from VIP.

Clustering of heading selectivity and perception-related activity in the ventral intraparietal area

The ventral intraparietal area (VIP) of the macaque brain is a multimodal cortical region, with many cells tuned to both optic flow and vestibular stimuli. Responses of many VIP neurons also show robust correlations with perceptual judgments during a fine heading discrimination task. Previous studies have shown that heading tuning based on optic flow is represented in a clustered fashion in VIP. However, it is unknown whether vestibular self-motion selectivity is clustered in VIP. Moreover, it is not known whether stimulus- and choice-related signals in VIP show clustering in the context of a heading discrimination task. To address these issues, we compared the response characteristics of isolated single units (SUs) with those of the undifferentiated multiunit (MU) activity corresponding to several neighboring neurons recorded from the same microelectrode. We find that MU activity typically shows selectivity similar to that of simultaneously recorded SUs, for both the vestibular and visual stimulus conditions. In addition, the choice-related activity of MU signals, as quantified using choice probabilities, is correlated with the choice-related activity of SUs. Overall, these findings suggest that both sensory and choice-related signals regarding self-motion are clustered in VIP. NEW & NOTEWORTHY We demonstrate, for the first time, that the vestibular tuning of ventral intraparietal area (VIP) neurons in response to both translational and rotational motion is clustered. In addition, heading discriminability and choice-related activity are also weakly clustered in VIP.

Visual selectivity for heading in the macaque ventral intraparietal area

The patterns of optic flow seen during self-motion can be used to determine the direction of one's own heading. Tracking eye movements which typically occur during everyday life alter this task since they add further retinal image motion and (predictably) distort the retinal flow pattern. Humans employ both visual and nonvisual (extraretinal) information to solve a heading task in such case. Likewise, it has been shown that neurons in the monkey medial superior temporal area (area MST) use both signals during the processing of self-motion information. In this article we report that neurons in the macaque ventral intraparietal area (area VIP) use visual information derived from the distorted flow patterns to encode heading during (simulated) eye movements. We recorded responses of VIP neurons to simple radial flow fields and to distorted flow fields that simulated self-motion plus eye movements. In 59% of the cases, cell responses compensated for the distortion and kept the same heading selectivity irrespective of different simulated eye movements. In addition, response modulations during real compared with simulated eye movements were smaller, being consistent with reafferent signaling involved in the processing of the visual consequences of eye movements in area VIP. We conclude that the motion selectivities found in area VIP, like those in area MST, provide a way to successfully analyze and use flow fields during self-motion and simultaneous tracking movements.