Transmodal nodes in midtemporal cortex, Wernicke's area, posterior parietal cortex, prefrontal cortex, amygdala, and the hippocampoentorhinal complex link distributed information into coherent multimodal assemblies necessary for face and object recognition, naming, working memory, spatial attention, emotional channeling, and explicit memory. These transmodal areas provide the cortical epicenters of large-scale distributed networks.
The pattern of connectivity summarized in Fig. 3 is based on anatomical experiments related to the network for spatial attention in the monkey and may reflect an organization that is common to all large-scale networks. In Fig. 3, A and B represent two interconnected epicenters of any large-scale neural network. They could represent the frontal eye fields and posterior parietal cortex in the network for spatial attention, midtemporal and temporopolar cortices in the network for face and object recognition, the amygdala and the hippocampoentorhinal complex in the emotion/memory network, Wernicke's area and Broca's area in the language network, and prefrontal cortex and posterior parietal cortex in the working memory/executive function network. Axonal transport experiments in the spatial attention network of the monkey indicate that if one member of such a pair, for example, A, is interconnected with additional cortical areas such as 1-3, then B is also interconnected with the same three cortical areas. Consequently, if A transmits a message, B will receive it directly but also through the alternative vantage points provided by areas 1-3. This arrangement enables parallel processing and contains multiple nodes where transitions
Figure 3 General organizational principles of large-scale neurocognitive networks.
between parallel and serial processing can occur. In resolving a complex cognitive problem such as reconstructing a past memory, selecting words to express a thought, or figuring out the identity of a face, a set of cortical areas interconnected in this fashion can execute an extremely rapid survey of a vast informational landscape while considering numerous goals, constraints, scenarios, and hypotheses until the entire system settles into a state of least conflict that becomes identified as the solution to the cognitive problem.
Because cortical areas tend to have very extensive corticocortical projections, individual sectors of association cortex are likely to belong to multiple intersecting networks. With rare exceptions, however, thalamic subnuclei have almost no connections among each other and some thalamic subnuclei can project to both epicenters of an individual large-scale neural network. Thalamic subnuclei can thus fulfill the very important role of setting coactivation boundaries for individual networks. Neuroanatomical experiments have shown that interconnected cortical areas are likely to send interdigitating projections to the stria-tum. Since the striatum receives cortical inputs but does not project back to the cerebral cortex, it could serve the role of an efference synchronizer (or filter) for coordinating the outputs of cortical areas in a given network. The human brain contains at least the following five large-scale neurocognitive networks that follow these principles of organization:
1. Dorsal parietofrontal network for spatial orientation: The cortices around the intraparietal sulcus and the frontal eye fields constitute the two major interconnected epicenters. The parietal component displays a relative specialization for the perceptual representation of salient events and their transformation into targets for attentional behaviors, and the frontal component displays a relative specialization for choosing and sequencing exploratory and orienting movements. Additional critical components are located in the cingulate gyrus, striatum, and thalamus. Damage to this network yields deficits of spatial attention and exploration such as contralesional hemispatial neglect, simultanagnosia, and other manifestations of spatial disorientation. Contralesional neglect occurs almost exclusively after right-sided damage to this network, whereas simultanagnosia tends to arise after bilateral lesions.
2. Limbic network for memory and emotion: The hippocampoentorhinal complex and the amygdala constitute the two interconnected epicenters. The former displays a relative specialization for memory and learning and the latter for drive, emotion, and visceral tone. Additional critical components are located in the paralimbic cortices, the hypothalamus, the limbic thalamus, and the limbic striatum. Damage to this network yields deficits of memory, emotion, affiliative behaviors, and autonomic regulation. Severe deficits usually occur only after bilateral lesions. Occasionally, unilateral left-sided lesions give rise to a multimodal amnesia but this is transient. Frequently, unilateral lesions in the left give rise to prominent deficits of verbal memory, whereas unilateral lesions on the right give rise to nonverbal memory deficits that are usually quite mild.
3. Perisylvian network for language: The two epicenters of this network are known as Broca's area and Wernicke's area. Broca's area includes the pre-motor region BA 44 and the adjacent heteromodal fields of BA 45-47; Wernicke's area includes the posterior part of auditory association cortex in BA 22 and also adjacent heteromodal fields in BA 39-40 and BA 21. Broca's area displays a relative specialization for the articulatory, syntactic, and grammatical aspects of language, whereas Wernicke's area displays a specialization for the lexical and semantic aspects. Additional components of this network are located in the striatum, thalamus, and the association areas of the frontal, temporal, and parietal lobes. Damage to this network yields aphasia, alexia, and agraphia. Such deficits are seen only after damage to the left hemisphere in the majority of the population.
4. Ventral occipitotemporal network for object recognition: The middle temporal gyrus and the temporal pole appear to contain the transmodal epicenters for this network. Additional critical components are located in the fusiform gyrus and inferior temporal gyrus. Damage to this network yields recognition deficits such as object agnosia and proso-pagnosia. The lesions that cause such deficits are almost always bilateral. The fusiform gyrus is the most common site of lesions, probably because it is the only part of this network with a vascular supply that makes bilateral damage likely. Occasionally, unilateral left-sided lesions can lead to object agnosia and unilateral right-sided lesions to prosopagnosia.
5. Prefrontal network for executive function and comportment: Prefrontal heteromodal cortex and orbitofrontal cortex are the major cortical epicenters involved in the coordination of comportment, working memory, and related executive functions. The head of the caudate nucleus and the mediodorsal nucleus of the thalamus constitute additional critical components. Deficits of comportment are frequently associated with lesions of orbitofrontal and adjacent medial frontal cortex, whereas deficits of executive function and working memory are frequently associated with damage to dorsolateral prefrontal cortex. Clinically significant deficits are usually seen only after bilateral lesions. Occasionally, unilateral left-sided lesions give rise to a syndrome of abulia, whereas unilateral right-sided lesions give rise to behavioral disinhibition.
Neuroanatomical experiments in the homologous regions of the monkey brain have shown that the components of these five networks are interconnected according to the pattern shown in Fig. 3. As noted previously, each of these networks receives its sensory information from a common set of unimodal cortical areas. The differences in the resultant cognitive functions are determined by the anatomical location and specializations of the relevant transmodal epicenters. The large-scale network approach predicts that many, if not all, network components will be activated in concert during the performance of any task in a given cognitive domain. In keeping with this prediction, tasks related to spatial awareness, language, working memory, explicit memory, and object identification in human subjects have led to the collective activation of the relevant epicenters noted previously. Functional imaging experiments cannot yet determine whether all network components are activated simultaneously or if the temporal sequence of activation varies according to the nature of the task. Such questions can be addressed by combining functional imaging with event-related potentials.
Large-scale neural networks are organized according to the principles of selectively distributed processing. For example, Wernicke's area occupies the lexical/semantic pole of the language network but also participates in articulation and syntax, whereas Bro-ca's area occupies the articulatory/syntactic pole ofthe network but also participates in phonological discrimination and lexical access. In the case of spatial attention, the frontal eye fields occupy the motor/ exploratory pole of the relevant network but also participate in the compilation of perceptual representations, whereas posterior parietal cortex occupies the sensory/representational pole but also participates in the programming of exploratory movements. In the limbic network, the hippocampal complex is most closely related to explicit memory but also plays a role in emotional modulation, whereas the amygdaloid complex is most closely related to emotional modula tion but also participates in the encoding of emotionally salient memories. This organization promotes flexibility without sacrificing regional functional segregation.
At least two levels of connectivity contribute to the functional organization of neurocognitive networks. At one level, genetically encoded and relatively fixed axonal connections specify the type of information that a given region will process. These connections determine the location and functional specialization of network components. At a second level, experience-induced modifications of synaptic strengths enable the gradual accumulation of an experiential base that is unique for each individual. This process is known as neuroplasticity. Although we tend to think of plasticity as a phenomenon confined to early development, dendritic and axonal remodeling occurs throughout life and allows each individual brain to establish new associations, adapt to new situations, and compensate for biological attrition. A deeper understanding of these more dynamic aspects of brain structure is a major goal of behavioral neuroscience.
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