Direct comparison of contralateral bias and face/scene selectivity in human occipitotemporal cortex

Human visual cortex is organised broadly according to two major principles: retinotopy (the spatial mapping of the retina in cortex) and category-selectivity (preferential responses to specific categories of stimuli). Historically, these principles were considered anatomically separate, with retinotopy restricted to the occipital cortex and category-selectivity emerging in the lateral-occipital and ventral-temporal cortex. However, recent studies show that category-selective regions exhibit systematic retinotopic biases, for example exhibiting stronger activation for stimuli presented in the contra- compared to the ipsilateral visual field. It is unclear, however, whether responses within category-selective regions are more strongly driven by retinotopic location or by category preference, and if there are systematic differences between category-selective regions in the relative strengths of these preferences. Here, we directly compare contralateral and category preferences by measuring fMRI responses to scene and face stimuli presented in the left or right visual field and computing two bias indices: a contralateral bias (response to the contralateral minus ipsilateral visual field) and a face/scene bias (preferred response to scenes compared to faces, or vice versa). We compare these biases within and between scene- and face-selective regions and across the lateral and ventral surfaces of the visual cortex more broadly. We find an interaction between surface and bias: lateral surface regions show a stronger contralateral than face/scene bias, whilst ventral surface regions show the opposite. These effects are robust across and within subjects, and appear to reflect large-scale, smoothly varying gradients. Together, these findings support distinct functional roles for the lateral and ventral visual cortex in terms of the relative importance of the spatial location of stimuli during visual information processing. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1007/s00429-021-02411-8

A Direct Demonstration of Functional Differences between Subdivisions of Human V5/MT

Two subdivisions of human V5/MT+: one located posteriorly (MT/TO-1) and the other more anteriorly (MST/TO-2) were identified in human participants using functional magnetic resonance imaging on the basis of their representations of the ipsilateral versus contralateral visual field. These subdivisions were then targeted for disruption by the application of repetitive transcranial magnetic stimulation (rTMS). The rTMS was delivered to cortical areas while participants performed direction discrimination tasks involving 3 different types of moving stimuli defined by the translational, radial, or rotational motion of dot patterns. For translational motion, performance was significantly reduced relative to baseline when rTMS was applied to both MT/TO-1 and MST/TO-2. For radial motion, there was a differential effect between MT/TO-1 and MST/TO-2, with only disruption of the latter area affecting performance. The rTMS failed to reveal a complete dissociation between MT/TO-1 and MST/TO-2 in terms of their contribution to the perception of rotational motion. On the basis of these results, MT/TO-1 and MST/TO-2 appear to be functionally distinct subdivisions of hV5/MT+. While both areas appear to be implicated in the processing of translational motion, only the anterior region (MST/TO-2) makes a causal contribution to the perception of radial motion

Transcranial magnetic stimulation to the occipital place area biases gaze during scene viewing

We can understand viewed scenes and extract task-relevant information within a few hundred milliseconds. This process is generally supported by three cortical regions that show selectivity for scene images: parahippocampal place area (PPA), medial place area (MPA) and occipital place area (OPA). Prior studies have focused on the visual information each region is responsive to, usually within the context of recognition or navigation. Here, we move beyond these tasks to investigate gaze allocation during scene viewing. Eye movements rely on a scene’s visual representation to direct saccades, and thus foveal vision. In particular, we focus on the contribution of OPA, which is i) located in occipito-parietal cortex, likely feeding information into parts of the dorsal pathway critical for eye movements, and ii) contains strong retinotopic representations of the contralateral visual field. Participants viewed scene images for 1034 ms while their eye movements were recorded. On half of the trials, a 500 ms train of five transcranial magnetic stimulation (TMS) pulses was applied to the participant’s cortex, starting at scene onset. TMS was applied to the right hemisphere over either OPA or the occipital face area (OFA), which also exhibits a contralateral visual field bias but shows selectivity for face stimuli. Participants generally made an overall left-to-right, top-to-bottom pattern of eye movements across all conditions. When TMS was applied to OPA, there was an increased saccade latency for eye movements toward the contralateral relative to the ipsilateral visual field after the final TMS pulse (400ms). Additionally, TMS to the OPA biased fixation positions away from the contralateral side of the scene compared to the control condition, while the OFA group showed no such effect. There was no effect on horizontal saccade amplitudes. These combined results suggest that OPA might serve to represent local scene information that can then be utilized by visuomotor control networks to guide gaze allocation in natural scenes

An enhanced role for right hV5/MT+ in the analysis of motion in the contra- and ipsi-lateral visual hemi-fields

Previous experiments have demonstrated that transcranial magnetic stimulation (TMS) of human V5/MT+, in either the left or right cerebral hemisphere, can induce deficits in visual motion perception in their respective contra- and ipsi-lateral visual hemi-fields. However, motion deficits in the ipsi-lateral hemi-field are greater when TMS is applied to V5/MT + in the right hemisphere relative to the left hemisphere. One possible explanation for this asymmetry might lie in differential stimulation of sub-divisions within V5/MT + across the two hemispheres. V5/MT + has two major sub-divisions; MT/TO-1 and MST/TO-2, the latter area contains neurons with large receptive fields (RFs) that extend up to 15° further into the ipsi-lateral hemi-field than the former. We wanted to examine whether applying TMS to MT/TO-1 and MST/TO-2 separately could explain the previously reported functional asymmetries for ipsi-lateral motion processing in V5/MT + across right and left cerebral hemispheres. MT/TO-1 and MST/TO-2 were identified in seven subjects using fMRI localisers. In psychophysical experiments subjects identified the translational direction (up/down) of coherently moving dots presented in either the left or right visual field whilst repetitive TMS (25 Hz; 70%) was applied synchronously with stimulus presentation. Application of TMS to MT/TO-1 and MST/TO-2 in the right hemisphere affected translational direction discrimination in both contra-lateral and ipsi-lateral visual fields. In contrast, deficits of motion perception following application of TMS to MT/TO-1 and MST/TO-2 in the left hemisphere were restricted to the contra-lateral visual field. This result suggests an enhanced role for the right hemisphere in processing translational motion across the full visual field

Retinotopy drives the variation in scene responses across visual field map divisions of the occipital place area

The occipital place area (OPA) is a scene-selective region on the lateral surface of human occipitotemporal cortex that spatially overlaps multiple visual field maps, as well as portions of cortex that are not currently defined as retinotopic. Here we combined population receptive field modeling and responses to scenes in a representational similarity analysis (RSA) framework to test the prediction that the OPA's visual field map divisions contribute uniquely to the overall pattern of scene selectivity within the OPA. Consistent with this prediction, the patterns of response to a set of complex scenes were heterogeneous between maps. To explain this heterogeneity, we tested the explanatory power of seven candidate models using RSA. These models spanned different scene dimensions (Content, Expanse, Distance), low- and high-level visual features, and navigational affordances. None of the tested models could account for the variation in scene response observed between the OPA's visual field maps. However, the heterogeneity in scene response was correlated with the differences in retinotopic profiles across maps. These data highlight the need to carefully examine the relationship between regions defined as category-selective and the underlying retinotopy, and they suggest that, in the case of the OPA, it may not be appropriate to conceptualize it as a single scene-selective region

Evaluating the correspondence between face-, scene-, and object-selectivity and retinotopic organization within lateral occipitotemporal cortex

The organization of human lateral occipitotemporal cortex (lOTC) has been characterized largely according to two distinct principles: retinotopy and category-selectivity. Whereas category-selective regions were originally thought to exist beyond retinotopic maps, recent evidence highlights overlap. Here, we combined detailed mapping of retinotopy, using population receptive fields (pRF), and category-selectivity to examine and contrast the retinotopic profiles of scene- (occipital place area, OPA), face- (occipital face area, OFA) and object- (lateral occipital cortex, LO) selective regions of lOTC. We observe striking differences in the relationship each region has to underlying retinotopy. Whereas OPA overlapped multiple retinotopic maps (including V3A, V3B, LO1, and LO2), and LO overlapped two maps (LO1 and LO2), OFA overlapped almost none. There appears no simple consistent relationship between category-selectivity and retinotopic maps, meaning category-selective regions are not constrained spatially to retinotopic map borders consistently. The multiple maps that overlap OPA suggests it is likely not appropriate to conceptualize it as a single scene-selective region, whereas the inconsistency in any systematic map overlapping OFA suggests it may constitute a more uniform area. Beyond their relationship to retinotopy, all three regions evidenced strongly retinotopic voxels, with pRFs exhibiting a significant bias towards the contralateral lower visual field, despite differences in pRF size, contributing to an emerging literature suggesting this bias is present across much of lOTC. Taken together, these results suggest that whereas category-selective regions are not constrained to consistently contain ordered retinotopic maps, they nonetheless likely inherit retinotopic characteristics of the maps from which they draw information

Differential processing of the direction and focus of expansion of optic flow stimuli in areas MST and V3A of the human visual cortex

Human neuropsychological and neuroimaging studies have raised the possibility that different attributes of optic flow stimuli, namely radial direction and the position of the focus of expansion (FOE), are processed within separate cortical areas. In the human brain, visual areas V5/MT+ and V3A have been proposed as integral to the analysis of these different attributes of optic flow stimuli. To establish direct causal relationships between neural activity in human (h)V5/MT+ and V3A and the perception of radial motion direction and FOE position, we used transcranial magnetic stimulation (TMS) to disrupt cortical activity in these areas while participants performed behavioral tasks dependent on these different aspects of optic flow stimuli. The cortical regions of interest were identified in seven human participants using standard functional MRI retinotopic mapping techniques and functional localizers. TMS to area V3A was found to disrupt FOE positional judgments but not radial direction discrimination, whereas the application of TMS to an anterior subdivision of hV5/MT+, MST/TO-2 produced the reverse effects, disrupting radial direction discrimination but eliciting no effect on the FOE positional judgment task. This double dissociation demonstrates that FOE position and radial direction of optic flow stimuli are signaled independently by neural activity in areas hV5/MT+ and V3A.NEW & NOTEWORTHY Optic flow constitutes a biologically relevant visual cue as we move through any environment. With the use of neuroimaging and brain-stimulation techniques, this study demonstrates that separate human brain areas are involved in the analysis of the direction of radial motion and the focus of expansion in optic flow. This dissociation reveals the existence of separate processing pathways for the analysis of different attributes of optic flow that are important for the guidance of self-locomotion and object avoidance