Winrich A. Freiwald

Faces and objects in macaque cerebral cortex

How are different object categories organized by the visual system? Current evidence indicates that monkeys and humans process object categories in fundamentally different ways. Functional magnetic resonance imaging (fMRI) studies suggest that humans have a ventral temporal face area, but such evidence is lacking in macaques. Instead, face-responsive neurons in macaques seem to be scattered throughout temporal cortex, with some relative concentration in the superior temporal sulcus (STS). Here, using fMRI in alert fixating macaque monkeys and humans, we found that macaques do have discrete face-selective patches, similar in relative size and number to face patches in humans. The face patches were embedded within a large swath of object-selective cortex extending from V4 to rostral TE. This large region responded better to pictures of intact objects compared to scrambled objects, with different object categories eliciting different patterns of activity, as in the human. Overall, our results suggest that humans and macaques share a similar brain architecture for visual object processing.

Patches with Links: A Unified System for Processing Faces in the Macaque Temporal Lobe

The brain processes objects through a series of regions along the ventral visual pathway, but the circuitry subserving the analysis of specific complex forms remains unknown. One complex form category, faces, selectively activates six patches of cortex in the macaque ventral pathway. To identify the connectivity of these face patches, we used electrical microstimulation combined with simultaneous functional magnetic resonance imaging. Stimulation of each of four targeted face patches produced strong activation, specifically within a subset of the other face patches. Stimulation outside the face patches produced an activation pattern that spared the face patches. These results suggest that the face patches form a strongly and specifically interconnected hierarchical network.

Stimulus dependent intercolumnar synchronization of single unit responses in cat area 17.

Recent concepts of cortical information processing suggest that visual stimuli are represented by ensembles of synchronously firing neurones. This hypothesis predicts that individual cells in separate columns of the visual cortex should synchronize their discharges in response to a single coherent stimulus and fire asynchronously when each neurone responds to a different stimulus. To test this prediction, we recorded simultaneously with two stereotrodes from single units with non-overlapping, colinearly arranged receptive fields in area 17 of the anaesthetized cat. In support of the hypothesis, cell pairs activated by the same long bar stimulus discharged in synchrony, and fired with no or diminished temporal correlation when each neurone was activated by an independent light bar.

Cingulate cortex: Diverging data from humans and monkeys

Cognitive neuroscience research relies, in part, on homologies between the brains of human and non-human primates. A quandary therefore arises when presumed anatomical homologues exhibit different functional properties. Such a situation has recently arisen in the case of the anterior cingulate cortex (ACC). In humans, numerous studies suggest a role for ACC in detecting conflicts in information processing. Studies of macaque monkey ACC, in contrast, have failed to find conflict-related responses. We consider several interpretations of this discrepancy, including differences in research methodology and cross-species differences in functional neuroanatomy. New directions for future research are outlined, emphasizing the importance of distinguishing illusory cross-species differences from the true evolutionary differences that make our species unique.

Functional Connectivity of the Macaque Brain across Stimulus and Arousal States

Cortical networks generate temporally correlated brain activity. To clarify the functional significance of this correlated activity, we asked whether and how its structure depends on stimulus and arousal state. Using independent components analysis of macaque functional magnetic resonance imaging data, we identified a large number of brain networks that were strikingly reproducible across different visual stimulus contexts. Fewer networks were reproducible across alert and anesthetized brain states. Network complexity ranged from bilateral single-node networks to networks comprising multiple discrete nodes distributed over 3 cm of cortex; one network identified in our survey included parts of the temporal parietal occipital junction, dorsal premotor cortex, insula, and posterior cingulate cortex bilaterally. Our results reveal the wealth of spatially structured correlated networks throughout the brain in both alert and anesthetized monkeys, and show that anesthesia significantly alters the spatial structure of these networks.

Face recognition systems in monkey and human: are they the same thing?

Primate societies are based on face recognition. Face recognition mechanisms have been studied most extensively in humans and macaque monkeys. In both species, multiple brain areas specialized for face processing have been found, and their functional properties are characterized with increasing detail, so we can now begin to address questions about similarities and differences of face-recognition systems across species with 25 million years of separate evolution. Both systems are organized into multiple face-selective cortical areas in spatial arrangements and with functional specializations, implying both hierarchical and parallel modes of information processing. Yet open questions about homologies remain. To address these, future studies employing similar techniques and experimental designs across multiple species are needed to identify a putative core primate face processing system and to understand its differentiations into the multiple branches of the primate order.

Faces in motion: selectivity of macaque and human face processing areas for dynamic stimuli.

Face recognition mechanisms need to extract information from static and dynamic faces. It has been hypothesized that the analysis of dynamic face attributes is performed by different face areas than the analysis of static facial attributes. To date, there is no evidence for such a division of labor in macaque monkeys. We used fMRI to determine specializations of macaque face areas for motion. Face areas in the fundus of the superior temporal sulcus responded to general object motion; face areas outside of the superior temporal sulcus fundus responded more to facial motion than general object motion. Thus, the macaque face-processing system exhibits regional specialization for facial motion. Human face areas, processing the same stimuli, exhibited specializations for facial motion as well. Yet the spatial patterns of facial motion selectivity differed across species, suggesting that facial dynamics are analyzed differently in humans and macaques.

The Influence of Sustained Selective Attention on Stimulus Selectivity in Macaque Visual Area MT

Remarkable alterations of perception during long-lasting attentional processes have been described in several recent studies. Although these findings have gained much interest, almost nothing is known about the modulation of neuronal responses during sustained attention. Therefore, we investigated the effect of prolonged selective attention on neuronal feature selectivity. Awake macaque monkeys were trained to perform a motion-tracking task that required attending one of two simultaneously presented moving bars for up to 15 sec. Extracellular recordings were obtained from neurons in macaque motion-sensitive middle temporal visual area (MT/V5). Under conditions of attention, we found high and constant direction selectivity over time. This was expressed by a strong and persistent response contrast between presentations of preferred and nonpreferred stimuli in successive motion cycles. With attention directed to another moving bar, neuronal responses to the behaviorally irrelevant stimulus became continuously less specific for the direction of motion. In particular, increasingly higher firing rates for motion in null direction caused a strong reduction of direction selectivity, which further increased with enhanced proximity between target and distracter bar. A passive condition experiment revealed that this reduction occurred only when motion remained the behaviorally relevant feature but disappeared when attention was withdrawn from this feature domain. Thus, sustained attention seems to stabilize direction selectivity of neurons in area MT against a time and competition-dependent degradation, whereas nonattended objects suffer from a reduced neuronal representation.

A dedicated network for social interaction processing in the primate brain

A brain region for social cognition Monkeys recognize social interactions and their meanings quickly and effortlessly. Little is known about the neural circuitry that underlies this understanding. Sliwa and Freiwald scanned monkey brains as the monkeys watched static or moving stimuli. A subset of brain areas was exclusively active during monkey-monkey interactions, as opposed to physical interactions between two objects. This network shares some of its components with the monkey mirror neuron system mapped previously by others and with a possible homolog of the human network involved in the theory of mind. Science, this issue p. 745 The primate brain devotes an entire network exclusively to the analysis of social interactions. Primate cognition requires interaction processing. Interactions can reveal otherwise hidden properties of intentional agents, such as thoughts and feelings, and of inanimate objects, such as mass and material. Where and how interaction analyses are implemented in the brain is unknown. Using whole-brain functional magnetic resonance imaging in macaque monkeys, we discovered a network centered in the medial and ventrolateral prefrontal cortex that is exclusively engaged in social interaction analysis. Exclusivity of specialization was found for no other function anywhere in the brain. Two additional networks, a parieto-premotor and a temporal one, exhibited both social and physical interaction preference, which, in the temporal lobe, mapped onto a fine-grain pattern of object, body, and face selectivity. Extent and location of a dedicated system for social interaction analysis suggest that this function is an evolutionary forerunner of human mind-reading capabilities.

Intelligent Information Loss: The Coding of Facial Identity, Head Pose, and Non-Face Information in the Macaque Face Patch System

Faces are a behaviorally important class of visual stimuli for primates. Recent work in macaque monkeys has identified six discrete face areas where most neurons have higher firing rates to images of faces compared with other objects (Tsao et al., 2006). While neurons in these areas appear to have different tuning (Freiwald and Tsao, 2010; Issa and DiCarlo, 2012), exactly what types of information and, consequently, which visual behaviors neural populations within each face area can support, is unknown. Here we use population decoding to better characterize three of these face patches (ML/MF, AL, and AM). We show that neural activity in all patches contains information that discriminates between the broad categories of face and nonface objects, individual faces, and nonface stimuli. Information is present in both high and lower firing rate regimes. However, there were significant differences between the patches, with the most anterior patch showing relatively weaker representation of nonface stimuli. Additionally, we find that pose-invariant face identity information increases as one moves to more anterior patches, while information about the orientation of the head decreases. Finally, we show that all the information we can extract from the population is present in patterns of activity across neurons, and there is relatively little information in the total activity of the population. These findings give new insight into the representations constructed by the face patch system and how they are successively transformed.