Brain, Vol 121, Issue 6 1013-1052, Copyright © 1998 by Oxford University Press
MM Mesulam
Sensory information undergoes extensive associative elaboration and
attentional modulation as it becomes incorporated into the texture of
cognition. This process occurs along a core synaptic hierarchy which
includes the primary sensory, upstream unimodal, downstream unimodal,
heteromodal, paralimbic and limbic zones of the cerebral cortex.
Connections from one zone to another are reciprocal and allow higher
synaptic levels to exert a feedback (top-down) influence upon earlier
levels of processing. Each cortical area provides a nexus for the
convergence of afferents and divergence of efferents. The resultant
synaptic organization supports parallel as well as serial processing, and
allows each sensory event to initiate multiple cognitive and behavioural
outcomes. Upstream sectors of unimodal association areas encode basic
features of sensation such as colour, motion, form and pitch. More complex
contents of sensory experience such as objects, faces, word-forms, spatial
locations and sound sequences become encoded within downstream sectors of
unimodal areas by groups of coarsely tuned neurons. The highest synaptic
levels of sensory-fugal processing are occupied by heteromodal, paralimbic
and limbic cortices, collectively known as transmodal areas. The unique
role of these areas is to bind multiple unimodal and other transmodal areas
into distributed but integrated multimodal representations. Transmodal
areas in the midtemporal cortex, Wernicke's area, the
hippocampal-entorhinal complex and the posterior parietal cortex provide
critical gateways for transforming perception into recognition, word-forms
into meaning, scenes and events into experiences, and spatial locations
into targets for exploration. All cognitive processes arise from analogous
associative transformations of similar sets of sensory inputs. The
differences in the resultant cognitive operation are determined by the
anatomical and physiological properties of the transmodal node that acts as
the critical gateway for the dominant transformation. Interconnected sets
of transmodal nodes provide anatomical and computational epicentres for
large-scale neurocognitive networks. In keeping with the principles of
selectively distributed processing, each epicentre of a large-scale network
displays a relative specialization for a specific behavioural component of
its principal neurospychological domain. The destruction of transmodal
epicentres causes global impairments such as multimodal anomia, neglect and
amnesia, whereas their selective disconnection from relevant unimodal areas
elicits modality-specific impairments such as prosopagnosia, pure word
blindness and category-specific anomias. The human brain contains at least
five anatomically distinct networks. The network for spatial awareness is
based on transmodal epicentres in the posterior parietal cortex and the
frontal eye fields; the language network on epicentres in Wernicke's and
Broca's areas; the explicit memory/emotion network on epicentres in the
hippocampal-entorhinal complex and the amygdala; the face-object
recognition network on epicentres in the midtemporal and temporopolar
cortices; and the working memory-executive function network on epicentres
in the lateral prefrontal cortex and perhaps the posterior parietal cortex.
Individual sensory modalities give rise to streams of processing directed
to transmodal nodes belonging to each of these networks. The fidelity of
sensory channels is actively protected through approximately four synaptic
levels of sensory-fugal processing. The modality-specific cortices at these
four synaptic levels encode the most veridical representations of
experience. Attentional, motivational and emotional modulations, including
those related to working memory, novelty-seeking and mental imagery, become
increasingly more pronounced within downstream components of unimodal
areas, where they help to create a highly edited subjective version of the
world. (ABSTRACT TRUNCATED)
REVIEWS
From sensation to cognition
Department of Neurology, Northwestern University Medical School, Chicago 60611, USA. mmesulam@nwu.edu
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