The Primate Working Memory Networks

By Constantinidis, Christos; Procyk, Emmanuel | Cognitive, Affective and Behavioral Neuroscience, December 2004 | Go to article overview

The Primate Working Memory Networks

Constantinidis, Christos, Procyk, Emmanuel, Cognitive, Affective and Behavioral Neuroscience

Working memory has long been associated with the prefrontal cortex, since damage to this brain area can critically impair the ability to maintain and update mnemonic information. Anatomical and physiological evidence suggests, however, that the prefrontal cortex is part of a broader network of interconnected brain areas involved in working memory. These include the parietal and temporal association areas of the cerebral cortex, cingulate and limbic areas, and subcortical structures such as the mediodorsal thalamus and the basal ganglia. Neurophysiological studies in primates confirm the involvement of areas beyond the frontal lobe and illustrate that working memory involves parallel, distributed neuronal networks. In this article, we review the current understanding of the anatomical organization of networks mediating working memory and the neural correlates of memory manifested in each of their nodes. The neural mechanisms of memory maintenance and the integrative role of the prefrontal cortex are also discussed.

Working memory is the term commonly used for the ability to maintain information in memory over a time span of a few seconds. Working memory constitutes a core component of higher cognitive functions including language, problem solving, and reasoning (Baddeley, 1992). Lesion studies first localized working memory functions in the cortical surface of the frontal lobe (Jacobsen, 1936; Milner, 1963). Neurophysiological recordings subsequently provided a neural correlate of working memory in the sustained discharges of neurons that persisted even after the offset of brief stimuli that monkeys were trained to remember and recall (Fuster & Alexander, 1971). Individual neurons represent particular features and spatial locations so that the activity of the prefrontal population can encode a remembered stimulus. The part of the visual space in which stimulus appearance can produce sustained activation has been termed the neuron's memory field, analogous to the receptive field of neurons that respond to sensory stimulation (Funahashi, Bruce, & Goldman-Rakic, 1989).

Neurons with memory-related responses have since been reported in multiple brain regions-for example, the inferior temporal and posterior parietal cortices, which are the end stages of the ventral and dorsal visual pathways, respectively (Andersen, Essick, & Siegel, 1987; Fuster & Jervey, 1981). The prefrontal cortex is reciprocally connected to these areas in a well organized and systematic fashion: The dorsal prefrontal cortex (areas 8 and 46) is interconnected with the posterior parietal cortex, whereas the ventral prefrontal cortex (areas 12 and 45) is linked to the inferior temporal cortex. On the basis of this organization, Patricia Goldman-Rakic (1988) proposed that working memory is mediated by the sustained activity of neurons in parallel, distributed cortical networks. More recently, imaging modalities (PET and fMRI) have verified the concurrent activation of multiple human brain areas during performance of cognitive tasks that engage working memory, confirming the findings of the monkey neurophysiological studies (Courtney, Ungerleider, Keil, & Haxby, 1997; Jonides et al., 1993; Ungerleider, Courtney, & Haxby, 1998).

Over the last decade, great progress has been made in understanding the organization of the working memory networks and the functional specialization of brain areas that constitute them. Here, we will provide an update of the anatomical and physiological details of the working memory networks, focusing on the brain of the rhesus monkey as the best studied model. The prefrontal cortex will be the point of origin for our review. We will examine the organization of the prefrontal cortex and its connections with the sensory pathways-namely, the ventral and dorsal visual pathways and the somatosensory, auditory, gustatory, and olfactory cortices. We will also examine the function of the medial temporal system and that of limbic and subcortical structures. …

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