Existing models propose that primate visual cortex is divided into two functionally distinct pathways. The ventral pathway computes the identity of an object; the dorsal pathway computes the location ...of an object, and the actions related to that object. Despite remaining influential, the two visual pathways model requires revision. Both human and non-human primate studies reveal the existence of a third visual pathway on the lateral brain surface. This third pathway projects from early visual cortex, via motion-selective areas, into the superior temporal sulcus (STS). Studies demonstrating that the STS computes the actions of moving faces and bodies (e.g., expressions, eye-gaze, audio-visual integration, intention, and mood) show that the third visual pathway is specialized for the dynamic aspects of social perception.
The two-visual pathway model of primate visual cortex needs to be updated. We propose the existence of a third visual pathway on the lateral brain surface that is anatomically segregated from the dorsal and ventral pathways.The third pathway exists in human and non-human primates. In humans, the third pathway projects from early visual cortex into the superior temporal sulcus (STS). In macaques the third pathway projects from early visual cortex into the dorsal bank and fundus of the STS.The third pathway has distinct functional properties. It selectively responds to moving faces and bodies. Visual field-mapping studies show that the third pathway responds to faces across the visual field to a greater extent than the ventral pathway.The third pathway computes a range of higher sociocognitive functions based on dynamic social cues. These include facial expression recognition, eye gaze discrimination, the audiovisual integration of speech, and interpreting the actions and behaviors of other biological organisms.
Perceptual decision making is the act of choosing one option or course of action from a set of alternatives on the basis of available sensory evidence. Thus, when we make such decisions, sensory ...information must be interpreted and translated into behaviour. Neurophysiological work in monkeys performing sensory discriminations, combined with computational modelling, has paved the way for neuroimaging studies that are aimed at understanding decision-related processes in the human brain. Here we review findings from human neuroimaging studies in conjunction with data analysis methods that can directly link decisions and signals in the human brain on a trial-by-trial basis. This leads to a new view about the neural basis of human perceptual decision-making processes.
The right middle fontal gyrus (MFG) has been proposed to be a site of convergence of the dorsal and ventral attention networks, by serving as a circuit-breaker to interrupt ongoing endogenous ...attentional processes in the dorsal network and reorient attention to an exogenous stimulus. Here, we probed the contribution of the right MFG to both endogenous and exogenous attention by comparing performance on an orientation discrimination task of a patient with a right MFG resection and a group of healthy controls. On endogenously cued trials, participants were shown a central cue that predicted with 90% accuracy the location of a subsequent peri-threshold Gabor patch stimulus. On exogenously cued trials, a cue appeared briefly at one of two peripheral locations, followed by a variable inter-stimulus interval (ISI; range 0-700 ms) and a Gabor patch in the same or opposite location as the cue. Behavioral data showed that for endogenous, and short ISI exogenous trials, valid cues facilitated responses compared to invalid cues, for both the patient and controls. However, at long ISIs, the patient exhibited difficulty in reverting to top-down attentional control, once the facilitatory effect of the exogenous cue had dissipated. When explicitly cued during long ISIs to attend to both stimulus locations, the patient was able to engage successfully in top-down control. This result indicates that the right MFG may play an important role in reorienting attention from exogenous to endogenous attentional control. Resting state fMRI data revealed that the right superior parietal lobule and right orbitofrontal cortex, showed significantly higher correlations with a left MFG seed region (a region tightly coupled with the right MFG in controls) in the patient relative to controls. We hypothesize that this paradoxical increase in cortical coupling represents a compensatory mechanism in the patient to offset the loss of function of the resected tissue in right prefrontal cortex.
There is growing consensus that accurate and efficient face recognition is mediated by a neural circuit composed of a posterior “core” and an anterior “extended” set of regions. Here, we characterize ...the distributed face network in human individuals with congenital prosopagnosia (CP)—a lifelong impairment in face processing—relative to that of matched controls. Using functional magnetic resonance imaging, we first uncover largely normal activation patterns in the posterior core face patches in CP. We also document normal activity of the amygdala (emotion processing) as well as normal or even enhanced functional connectivity between the amygdala and the core regions. Critically, in the same individuals, activation of the anterior temporal cortex (identity processing) is reduced and connectivity between this region and the posterior core regions is disrupted. The dissociation between the neural profiles of the anterior temporal lobe and amygdala was evident both during a task-related face scan and during a resting state scan, in the absence of visual stimulation. Taken together, these findings elucidate selective disruptions in neural circuitry in CP and offer an explanation for the known differential difficulty in identity versus emotional expression recognition in many individuals with CP.
Since the original characterization of the ventral visual pathway, our knowledge of its neuroanatomy, functional properties, and extrinsic targets has grown considerably. Here we synthesize this ...recent evidence and propose that the ventral pathway is best understood as a recurrent occipitotemporal network containing neural representations of object quality both utilized and constrained by at least six distinct cortical and subcortical systems. Each system serves its own specialized behavioral, cognitive, or affective function, collectively providing the raison d’être for the ventral visual pathway. This expanded framework contrasts with the depiction of the ventral visual pathway as a largely serial staged hierarchy culminating in singular object representations and more parsimoniously incorporates attentional, contextual, and feedback effects.
•A network of cortical patches with curvature response preferences was observed in the human ventral visual stream.•Each curvature-preferring patch was involved in processing different curvilinear ...information.•Principal component analysis indicated that curvilinear information was associated with specific retinotopic visual regions.•Broad areas of curvature preference were bound by central visual field representations.•Areas of rectilinear preference were situated in peripheral visual field representations.
Curvature is one of many visual features shown to be important for visual perception. We recently showed that curvilinear features provide sufficient information for categorizing animate vs. inanimate objects, while rectilinear features do not (Zachariou et al., 2018). Results from our fMRI study in rhesus monkeys (Yue et al., 2014) have shed light on some of the neural substrates underlying curvature processing by revealing a network of visual cortical patches with a curvature response preference. However, it is unknown whether a similar network exists in human visual cortex. Thus, the current study was designed to investigate cortical areas with a preference for curvature in the human brain using fMRI at 7T. Consistent with our monkey fMRI results, we found a network of curvature preferring cortical patches—some of which overlapped well-known face-selective areas. Moreover, principal component analysis (PCA) using all visually-responsive voxels indicated that curvilinear features of visual stimuli were associated with specific retinotopic regions in visual cortex. Regions associated with positive curvilinear PC values encompassed the central visual field representation of early visual areas and the lateral surface of temporal cortex, while those associated with negative curvilinear PC values encompassed the peripheral visual field representation of early visual areas and the medial surface of temporal cortex. Thus, we found that broad areas of curvature preference, which encompassed face-selective areas, were bound by central visual field representations. Our results support the hypothesis that curvilinearity preference interacts with central-peripheral processing biases as primary features underlying the organization of temporal cortex topography in the adult human brain.
Feature-based attention has a spatially global effect, i.e., responses to stimuli that share features with an attended stimulus are enhanced not only at the attended location but throughout the ...visual field. However, how feature-based attention modulates cortical neural responses at unattended locations remains unclear. Here we used functional magnetic resonance imaging (fMRI) to examine this issue as human participants performed motion- (Experiment 1) and color- (Experiment 2) based attention tasks. Results indicated that, in both experiments, the respective visual processing areas (middle temporal area MT+ for motion and V4 for color) as well as early visual, parietal, and prefrontal areas all showed the classic feature-based attention effect, with neural responses to the unattended stimulus significantly elevated when it shared the same feature with the attended stimulus. Effective connectivity analysis using dynamic causal modeling (DCM) showed that this spatially global effect in the respective visual processing areas (MT+ for motion and V4 for color), intraparietal sulcus (IPS), frontal eye field (FEF), medial frontal gyrus (mFG), and primary visual cortex (V1) was derived by feedback from the inferior frontal junction (IFJ). Complementary effective connectivity analysis using Granger causality modeling (GCM) confirmed that, in both experiments, the node with the highest outflow and netflow degree was IFJ, which was thus considered to be the source of the network. These results indicate a source for the spatially global effect of feature-based attention in the human prefrontal cortex.
Nonhuman primate neuroanatomical studies have identified a cortical pathway from the superior temporal sulcus (STS) projecting into dorsal subregions of the amygdala, but whether this same pathway ...exists in humans is unknown. Here, we addressed this question by combining theta burst transcranial magnetic stimulation (TBS) with fMRI to test the prediction that the STS and amygdala are functionally connected during face perception. Human participants (N = 17) were scanned, over two sessions, while viewing 3 s video clips of moving faces, bodies, and objects. During these sessions, TBS was delivered over the face-selective right posterior STS (rpSTS) or over the vertex control site. A region-of-interest analysis revealed results consistent with our hypothesis. Namely, TBS delivered over the rpSTS reduced the neural response to faces (but not to bodies or objects) in the rpSTS, right anterior STS (raSTS), and right amygdala, compared with TBS delivered over the vertex. By contrast, TBS delivered over the rpSTS did not significantly reduce the neural response to faces in the right fusiform face area or right occipital face area. This pattern of results is consistent with the existence of a cortico-amygdala pathway in humans for processing face information projecting from the rpSTS, via the raSTS, into the amygdala. This conclusion is consistent with nonhuman primate neuroanatomy and with existing face perception models.
Neuroimaging studies have identified multiple face-selective regions in the brain, but the functional connections between these regions are unknown. In the present study, participants were scanned with fMRI while viewing movie clips of faces, bodies, and objects before and after transient disruption of the face-selective right posterior superior temporal sulcus (rpSTS). Results showed that TBS disruption reduced the neural response to faces, but not to bodies or objects, in the rpSTS, right anterior STS (raSTS), and right amygdala. These results are consistent with the existence of a cortico-amygdala pathway in humans for processing face information projecting from the rpSTS, via the raSTS, into the amygdala. This conclusion is consistent with nonhuman primate neuroanatomy and with existing face perception models.
It is widely held that the frontal eye field (FEF) in prefrontal cortex (PFC) modulates processing in visual cortex with attention, although the evidence that it is necessary is equivocal. To help ...identify critical sources of attentional feedback to area V4, we surgically removed the entire lateral PFC, including the FEF, in one hemisphere and transected the corpus callosum and anterior commissure in two macaques. This deprived V4 of PFC input in one hemisphere while keeping the other hemisphere intact. In the absence of PFC, attentional effects on neuronal responses and synchrony in V4 were substantially reduced and the remaining effects of attention were delayed in time, indicating a critical role for PFC. Conversely, distracters captured attention and influenced V4 responses. However, because the effects of attention in V4 were not eliminated by PFC lesions, other sources of top-down attentional control signals to visual cortex must exist outside of PFC.
Facial motion plays a fundamental role in the recognition of facial expressions in primates, but the neural substrates underlying this special type of biological motion are not well understood. Here, ...we used fMRI to investigate the extent to which the specialization for facial motion is represented in the visual system and compared the neural mechanisms for the processing of non-rigid facial motion in macaque monkeys and humans. We defined the areas specialized for facial motion as those significantly more activated when subjects perceived the motion caused by dynamic faces (dynamic faces > static faces) than when they perceived the motion caused by dynamic non-face objects (dynamic objects > static objects). We found that, in monkeys, significant activations evoked by facial motion were in the fundus of anterior superior temporal sulcus (STS), which overlapped the anterior fundus face patch. In humans, facial motion activated three separate foci in the right STS: posterior, middle, and anterior STS, with the anterior STS location showing the most selectivity for facial motion compared with other facial motion areas. In both monkeys and humans, facial motion shows a gradient preference as one progresses anteriorly along the STS. Taken together, our results indicate that monkeys and humans share similar neural substrates within the anterior temporal lobe specialized for the processing of non-rigid facial motion.
•We found facial-motion selectivity in the fundus of aSTS with monkey fMRI.•We found facial-motion selectivity in aSTS, mSTS and pSTS with human fMRI.•In both monkeys and humans, facial motion shows a gradient preference along the STS.•Monkeys and humans share similar neural substrates within aSTS for facial motion.
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