A Bartels

The neural basis of romantic love

The neural correlates of many emotional states have been studied, most recently through the technique of fMRI. However, nothing is known about the neural substrates involved in evoking one of the most overwhelming of all affective states, that of romantic love, about which we report here. The activity in the brains of 17 subjects who were deeply in love was scanned using fMRI, while they viewed pictures of their partners, and compared with the activity produced by viewing pictures of three friends of similar age, sex and duration of friendship as their partners. The activity was restricted to foci in the medial insula and the anterior cingulate cortex and, subcortically, in the caudate nucleus and the putamen, all bilaterally. Deactivations were observed in the posterior cingulate gyrus and in the amygdala and were right-lateralized in the prefrontal, parietal and middle temporal cortices. The combination of these sites differs from those in previous studies of emotion, suggesting that a unique network of areas is responsible for evoking this affective state. This leads us to postulate that the principle of functional specialization in the cortex applies to affective states as well.

The architecture of the colour centre in the human visual brain: new results and a review*

We have used the technique of functional magnetic resonance imaging (fMRI) and a variety of colour paradigms to activate the human brain regions selective for colour. We show here that the region defined previously [ Lueck et al. (1989) Nature, 340, 386–389; Zeki et al. (1991) J. Neurosci., 11, 641–649; McKeefry & Zeki (1997) Brain, 120, 2229–2242] as the human colour centre consists of two subdivisions, a posterior one, which we call V4 and an anterior one, which we refer to as V4α, the two together being part of the V4‐complex. The posterior area is retinotopically organized while the anterior is not. We discuss our new findings in the context of previous studies of the cortical colour processing system in humans and monkeys. Our new insight into the organization of the colour centre in the human brain may also account for the variability in both severity and degree of recovery from lesions producing cerebral colour blindness (achromatopsia).

Toward a Theory of Visual Consciousness

The visual brain consists of several parallel, functionally specialized processing systems, each having several stages (nodes) which terminate their tasks at different times; consequently, simultaneously presented attributes are perceived at the same time if processed at the same node and at different times if processed by different nodes. Clinical evidence shows that these processing systems can act fairly autonomously. Damage restricted to one system compromises specifically the perception of the attribute that that system is specialized for; damage to a given node of a processing system that leaves earlier nodes intact results in a degraded perceptual capacity for the relevant attribute, which is directly related to the physiological capacities of the cells left intact by the damage. By contrast, a system that is spared when all others are damaged can function more or less normally. Moreover, internally created visual percepts-illusions, afterimages, imagery, and hallucinations-activate specifically the nodes specialized for the attribute perceived. Finally, anatomical evidence shows that there is no final integrator station in the brain, one which receives input from all visual areas; instead, each node has multiple outputs and no node is recipient only. Taken together, the above evidence leads us to propose that each node of a processing-perceptual system creates its own microconsciousness. We propose that, if any binding occurs to give us our integrated image of the visual world, it must be a binding between microconsciousnesses generated at different nodes. Since any two microconsciousnesses generated at any two nodes can be bound together, perceptual integration is not hierarchical, but parallel and postconscious. By contrast, the neural machinery conferring properties on those cells whose activity has a conscious correlate is hierarchical, and we refer to it as generative binding, to distinguish it from the binding that might occur between the microconsciousnesses.

Functional brain mapping during free viewing of natural scenes.

Previous imaging studies have used mostly perceptually abstracted, idealized, or static stimuli to show segregation of function in the cerebral cortex. We wanted to learn whether functional segregation is maintained during more natural, complex, and dynamic conditions when many features have to be processed simultaneously, and identify regions whose activity correlates with the perception of specific features. To achieve this, we used functional magnetic resonance imaging (fMRI) to measure brain activity when human observers viewed freely dynamic natural scenes (a James Bond movie). The intensity with which they perceived different features (color, faces, language, and human bodies) was assessed psychometrically in separate sessions. In all subjects different features were perceived with a high degree of independence over time. We found that the perception of each feature correlated with activity in separate, specialized areas whose activity also varied independently. We conclude that even in natural conditions, when many features have to be processed simultaneously, functional specialization is preserved. Our method thus opens a new way of brain mapping, which allows the localization of a multitude of brain areas based on a single experiment using uncontrolled, natural stimuli. Furthermore, our results show that the intensity of activity in a specialized area is linearly correlated with the intensity of its perceptual experience. This leads us to suggest that each specialized area is directly responsible for the creation of a feature‐specific conscious percept (a microconsciousness). Hum. Brain Mapp. 21:75–83, 2004.

fMRI and its interpretations: an illustration on directional selectivity in area V5/MT

fMRI is a tool to study brain function noninvasively that can reliably identify sites of neural involvement for a given task. However, to what extent can fMRI signals be related to measures obtained in electrophysiology? Can the blood-oxygen-level-dependent signal be interpreted as spatially pooled spiking activity? Here we combine knowledge from neurovascular coupling, functional imaging and neurophysiology to discuss whether fMRI has succeeded in demonstrating one of the most established functional properties in the visual brain, namely directional selectivity in the motion-processing region V5/MT+. We also discuss differences of fMRI and electrophysiology in their sensitivity to distinct physiological processes. We conclude that fMRI constitutes a complement, not a poor-resolution substitute, to invasive techniques, and that it deserves interpretations that acknowledge its stand as a separate signal.

THE ASYNCHRONY OF CONSCIOUSNESS

We present below a simple hypothesis on what we believe is a characteristic of visual consciousness. It is derived from facts about the visual brain revealed in the past quarter of a century, but it relies most especially on psychophysical evidence which shows that different attributes of the visual scene are consciously perceived at different times. This temporal asynchrony in visual perception reveals, we believe, a plurality of visual consciousnesses that are asynchronous with respect to each other, reflecting the modular organization of the visual brain. We further hypothesize that when two attributes (e.g. colour and motion) are presented simultaneously, the activity of cells in a given processing system is sufficient to create a conscious experience of the corresponding attribute (e.g. colour), without the necessity for interaction with the activities of cells in other processing systems (e.g. motion). Thus, any binding of the activity of cells in different systems should be more properly thought of as a binding of the conscious experiences generated in each system.

Disrupting Parietal Function Prolongs Dominance Durations in Binocular Rivalry

Human brain imaging studies of bistable perceptual phenomena revealed that frontal and parietal areas are activated during perceptual switches between the two conflicting percepts. However, these studies do not provide information about causality, i.e., whether activity reports a consequence or a cause of the perceptual change. Here we used functional magnetic resonance imaging to individually localize four parietal regions involved in perceptual switches during binocular rivalry in 15 subjects and subsequently disturbed their neural processing and that of a control site using 2 Hz repetitive transcranial magnetic stimulation (TMS) during binocular rivalry. We found that TMS over one of the sites, the right intraparietal sulcus (IPS), prolonged the periods of stable percepts. Additionally, the more lateralized the blood oxygen level-dependent signal was in IPS, the more lateralized the TMS effects were. Lateralization varied considerably across subjects, with a right-hemispheric bias. Control replay experiments rule out nonspecific effects of TMS on task performance, reaction times, or eye blinks. Our results thus demonstrate a causal, destabilizing, and individually lateralized effect of normal IPS function on perceptual continuity in rivalry. This is in accord with a role of IPS in perceptual selection, relating its role in rivalrous perception to that in attention.

The chronoarchitecture of the cerebral cortex

We review here a new approach to mapping the human cerebral cortex into distinct subdivisions. Unlike cytoarchitecture or traditional functional imaging, it does not rely on specific anatomical markers or functional hypotheses. Instead, we propose that the unique activity time course (ATC) of each cortical subdivision, elicited during natural conditions, acts as a temporal fingerprint that can be used to segregate cortical subdivisions, map their spatial extent, and reveal their functional and potentially anatomical connectivity. We argue that since the modular organisation of the brain and its connectivity evolved and developed in natural conditions, these are optimal for revealing its organisation. We review the concepts, methodology and first results of this approach, relying on data obtained with functional magnetic resonance imaging (fMRI) when volunteers viewed traditional stimuli or a James Bond movie. Independent component analysis (ICA) was used to identify voxels belonging to distinct functional subdivisions, based on their differential spatio-temporal fingerprints. Many more regions could be segregated during natural viewing, demonstrating that the complexity of natural stimuli leads to more differential responses in more functional modules. We demonstrate that, in a single experiment, a multitude of distinct regions can be identified across the whole brain, even within the visual cortex, including areas V1, V4 and V5. This differentiation is based entirely on the differential ATCs of different areas during natural viewing. Distinct areas can therefore be identified without any a priori hypothesis about their function or spatial location. The areas we identified corresponded anatomically across subjects, and their ATCs showed highly area-specific inter-subject correlations. Furthermore, natural conditions led to a significant de-correlation of interregional ATCs compared to rest, indicating an increase in regional specificity during natural conditions. In contrast, the correlation between ATCs of distant regions of known substantial anatomical connections increased and reflected their known anatomical connectivity pattern. We demonstrate this using the example of the language network involving Brocas and Wernickes area and homologous areas in the two hemispheres. In conclusion, this new approach to brain mapping may not only serve to identify novel functional subdivisions, but to reveal their connectivity as well.

The theory of multistage integration in the visual brain

The theory of multistage integration is based on evidence that the visual brain consists of several parallel multistage processing systems, each specialized for a given attribute such as colour or motion. Each stage of a given system processes information at a distinct level of complexity. Our theory supposes that activity at any stage of a given multistage processing system is perceptually explicit: that is to say, it requires no further processing to generate a conscious experience. This activity can be integrated, or bound, with the perceptually explicit activity at any given stage of another or the same multistage processing system. Such binding is therefore not a process that generates a conscious experience, but rather one that brings different conscious experiences together. Many perceptual advantages result from such a flexible and dynamic integrative system. Conversely, there would be disadvantages to limiting perception and binding to hypothetical ‘terminal’ stages of such processing systems or to hypothetical ‘integrator’ areas. Although we formulate our hypothesis in terms of the visual brain, we believe it might form a general principle of brain functioning.

The temporal order of binding visual attributes

The brain processes distinct attributes such as colour and motion in anatomically largely segregated systems. Moreover, these two attributes are perceived with different latencies. Here, we show that the time required to bind these two attributes differs too. In psychophysical experiments, we determined minimal presentation times required to perceptually pair spatially separate pairs of stimuli consisting of colour or motion. Binding two colours required longer presentation times than binding the directions of two moving stimuli. Cross-attribute binding between colour and motion took longer than within-attribute binding. This was so even when the relative perceptual delay between colour and motion was compensated for, which accelerated colour-motion binding. Moreover, stimuli could be discriminated but not bound at fast presentation rates. Our results thus show that spatial binding is an attribute-specific process and faster within the same than across different attributes. Furthermore, the time required to bind attributes is independent of that required to process them, since colour is perceived before motion but requires longer time for binding. Finally, our results suggest that binding acts on attribute-specific neural representations of the stimuli at a late, perceptually explicit stage. These results lead us to conclude that spatial binding is separate from, and subsequent to, stimulus processing and that it is an attribute-dependent and post-conscious process.