Uri Hasson

Center-periphery organization of human object areas.

The organizing principles that govern the layout of human object-related areas are largely unknown. Here we propose a new organizing principle in which object representations are arranged according to a central versus peripheral visual field bias. The proposal is based on the finding that building-related regions overlap periphery-biased visual field representations, whereas face-related regions are associated with center-biased representations. Furthermore, the eccentricity maps encompass essentially the entire extent of object-related occipito-temporal cortex, indicating that most object representations are organized with respect to retinal eccentricity. A control experiment ruled out the possibility that the results are due exclusively to unequal feature distribution in these images. We hypothesize that brain regions representing object categories that rely on detailed central scrutiny (such as faces) are more strongly associated with processing of central information, compared to representations of objects that may be recognized by more peripheral information (such as buildings or scenes).

Eccentricity Bias as an Organizing Principle for Human High-Order Object Areas

We have recently proposed a center-periphery organization based on resolution needs, in which objects engaging in recognition processes requiring central-vision (e.g., face-related) are associated with center-biased representations, while objects requiring large-scale feature integration (e.g., buildings) are associated with periphery-biased representations. Here we tested this hypothesis by comparing the center-periphery organization with activations to five object categories: faces, buildings, tools, letter strings, and words. We found that faces, letter strings, and words were mapped preferentially within the center-biased representation. Faces showed a hemispheric lateralization opposite to that of letter strings and words. In contrast, buildings were mapped mainly to the periphery-biased representation, while tools activated both central and peripheral representations. The results are compatible with the notion that center-periphery organization allows the optimal allocation of cortical magnification to the specific requirements of various recognition processes.

The topography of high-order human object areas

Cortical topography is one of the most fundamental organizing principles of cortical areas. One such topography - eccentricity mapping - is present even in high-order, ventral stream visual areas. Within these areas, different object categories have specific eccentricity biases. In particular, faces, letters and words appear to be associated with central visual-field bias, whereas buildings are associated with a peripheral one. We propose that resolution needs are an important factor in organizing object representations: objects whose recognition depends on analysis of fine detail will be associated with central-biased representations, whereas objects whose recognition entails large-scale integration will be more peripherally biased.

Speaker–listener neural coupling underlies successful communication

Verbal communication is a joint activity; however, speech production and comprehension have primarily been analyzed as independent processes within the boundaries of individual brains. Here, we applied fMRI to record brain activity from both speakers and listeners during natural verbal communication. We used the speakers spatiotemporal brain activity to model listeners’ brain activity and found that the speakers activity is spatially and temporally coupled with the listeners activity. This coupling vanishes when participants fail to communicate. Moreover, though on average the listeners brain activity mirrors the speakers activity with a delay, we also find areas that exhibit predictive anticipatory responses. We connected the extent of neural coupling to a quantitative measure of story comprehension and find that the greater the anticipatory speaker–listener coupling, the greater the understanding. We argue that the observed alignment of production- and comprehension-based processes serves as a mechanism by which brains convey information.

Brain-to-brain coupling: a mechanism for creating and sharing a social world.

Cognition materializes in an interpersonal space. The emergence of complex behaviors requires the coordination of actions among individuals according to a shared set of rules. Despite the central role of other individuals in shaping ones mind, most cognitive studies focus on processes that occur within a single individual. We call for a shift from a single-brain to a multi-brain frame of reference. We argue that in many cases the neural processes in one brain are coupled to the neural processes in another brain via the transmission of a signal through the environment. Brain-to-brain coupling constrains and shapes the actions of each individual in a social network, leading to complex joint behaviors that could not have emerged in isolation.

Large-Scale Mirror-Symmetry Organization of Human Occipito-Temporal Object Areas

We have combined functional maps of retinotopy (eccentricity and meridian mapping), object category, and motion in a group of subjects to explore the large-scale topography of higher-order object areas. Our results reveal seven consistent category-related entities situated in the occipito-temporal cortex adjoining early visual areas. These include two face-related regions, three object-related regions, and two building-related regions. Interestingly, this complex category-related pattern is organized in a large-scale dorso-ventral mirror symmetry of object category. Furthermore, correlating this pattern to the map of visual field eccentricity, we found that the entire network of areas could be related to a single and unified eccentricity map. We hypothesize that this large-scale organization points to a possible development of high-order object areas through extension and specialization of a single proto-representation.

A Hierarchy of Temporal Receptive Windows in Human Cortex

Real-world events unfold at different time scales and, therefore, cognitive and neuronal processes must likewise occur at different time scales. We present a novel procedure that identifies brain regions responsive to sensory information accumulated over different time scales. We measured functional magnetic resonance imaging activity while observers viewed silent films presented forward, backward, or piecewise-scrambled in time. Early visual areas (e.g., primary visual cortex and the motion-sensitive area MT+) exhibited high response reliability regardless of disruptions in temporal structure. In contrast, the reliability of responses in several higher brain areas, including the superior temporal sulcus (STS), precuneus, posterior lateral sulcus (LS), temporal parietal junction (TPJ), and frontal eye field (FEF), was affected by information accumulated over longer time scales. These regions showed highly reproducible responses for repeated forward, but not for backward or piecewise-scrambled presentations. Moreover, these regions exhibited marked differences in temporal characteristics, with LS, TPJ, and FEF responses depending on information accumulated over longer durations (∼36 s) than STS and precuneus (∼12 s). We conclude that, similar to the known cortical hierarchy of spatial receptive fields, there is a hierarchy of progressively longer temporal receptive windows in the human brain.

Reliability of cortical activity during natural stimulation

Response reliability is complementary to more conventional measurements of response amplitudes, and can reveal phenomena that response amplitudes do not. Here we review studies that measured reliability of cortical activity within or between human subjects in response to naturalistic stimulation (e.g. free viewing of movies). Despite the seemingly uncontrolled nature of the task, some of these complex stimuli evoke highly reliable, selective and time-locked activity in many brain areas, including some regions that show little response modulation in most conventional experimental protocols. This activity provides an opportunity to address novel questions concerning natural vision, temporal scale of processing, memory and the neural basis of inter-group differences.

Topographic Mapping of a Hierarchy of Temporal Receptive Windows Using a Narrated Story

Real-life activities, such as watching a movie or engaging in conversation, unfold over many minutes. In the course of such activities, the brain has to integrate information over multiple time scales. We recently proposed that the brain uses similar strategies for integrating information across space and over time. Drawing a parallel with spatial receptive fields, we defined the temporal receptive window (TRW) of a cortical microcircuit as the length of time before a response during which sensory information may affect that response. Our previous findings in the visual system are consistent with the hypothesis that TRWs become larger when moving from low-level sensory to high-level perceptual and cognitive areas. In this study, we mapped TRWs in auditory and language areas by measuring fMRI activity in subjects listening to a real-life story scrambled at the time scales of words, sentences, and paragraphs. Our results revealed a hierarchical topography of TRWs. In early auditory cortices (A1+), brain responses were driven mainly by the momentary incoming input and were similarly reliable across all scrambling conditions. In areas with an intermediate TRW, coherent information at the sentence time scale or longer was necessary to evoke reliable responses. At the apex of the TRW hierarchy, we found parietal and frontal areas that responded reliably only when intact paragraphs were heard in a meaningful sequence. These results suggest that the time scale of processing is a functional property that may provide a general organizing principle for the human cerebral cortex.

Detailed Exploration of Face-related Processing in Congenital Prosopagnosia: 2. Functional Neuroimaging Findings

Specific regions of the human occipito-temporal cortex are consistently activated in functional imaging studies of face processing. To understand the contribution of these regions to face processing, we examined the pattern of fMRI activation in four congenital prosopagnosic (CP) individuals who are markedly impaired at face processing despite normal vision and intelligence, and with no evidence of brain damage. These individuals evinced a normal pattern of fMRI activation in the fusiform gyrus (FFA) and in other ventral occipito-temporal areas, in response to faces, buildings, and other objects, shown both as line drawings in detection and discrimination tasks and under more naturalistic testing conditions when no task was required. CP individuals also showed normal adaptation levels in a block-design adaptation experiment and, like control subjects, exhibited evidence of global face representation in the FFA. The absence of a BOLD-behavioral correlation (profound behavioral deficit, normal face-related activation in the ventral occipito-temporal cortex) challenges existing accounts of face representation, and suggests that activation in these cortical regions per se is not sufficient to ensure intact face processing.