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posted 03. December 2004 23:38
PLoS Biology. Volume 2, Issue 11, November 2004
Representation of Attended Versus Remembered Locations in Prefrontal Cortex
Mikhail A. Lebedev, Adam Messinger, Jerald D. Kralik, Steven P. Wise
Abstract
A great deal of research on the prefrontal cortex^ (PF), especially in nonhuman primates, has focused on the theory that it functions predominantly in the maintenance of short-term memories, and neurophysiologists have often interpreted PF's delay-period activity in the context of this theory. Neuroimaging results, however, suggest that PF's function extends beyond the maintenance of memories to include aspects of attention, such as the monitoring and selection of information. To explore alternative interpretations of PF's delay-period activity, we investigated the discharge rates of single PF neurons as monkeys attended to a stimulus marking one location while remembering a different, unmarked location. Both locations served as potential targets of a saccadic eye movement. Although the task made intensive demands on short-term memory, the largest proportion of PF neurons represented attended locations, not remembered ones. The present findings show that short-term memory functions cannot account for all, or even most, delay-period activity in the part of PF explored. Instead, PF's delay-period activity probably contributes more to the process of attentional selection.
Received April 28, 2004; Accepted August 23, 2004; Published October 26, 2004
DOI: 10.1371/journal.pbio.0020365
This is an open-access article distributed under the terms of the Creative Commons Public Domain Declaration, which stipulates that, once placed in the public domain, this work may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose.
Abbreviations: Att-trial, attended-location trial; IAtt, attended-location index; IQR, interquartile range; IRem, remembered-location index; PETH, peri-event time histogram; PF, prefrontal cortex; PFdl, dorsolateral prefrontal cortex; Rem-trial, remembered-location trial
Academic Editor: Wolfram Schultz, University of Cambridge
*To whom correspondence should be addressed. E-mail: lebedev@neuro.duke.edu
Current address: Center for Neuroengineering, Department of Neurobiology, Duke University Medical Center, Durham, North Carolina, United States of America
Citation: Lebedev MA, Messinger A, Kralik JD, Wise SP (2004) Representation of Attended Versus Remembered Locations in Prefrontal Cortex. PLoS Biol 2(11): e365.
Introduction - Paragraphs 3-6
Consistent with the idea that PF functions predominantly in maintenance memory, delay-period activity in PF has often been interpreted as a memory trace (e.g., Funahashi et al. 1989; Romo et al. 1999; Constantinidis et al. 2001). The phrase delay-period activity applies to neuronal activity that follows the transient presentation of an instruction cue and persists until a subsequent “go” or “trigger” signal. The description of delay-period activity in PFdl appeared very early in the history of behavioral neurophysiology (Fuster and Alexander 1971; Kubota and Niki 1971; Fuster 1973), and, in accord with the maintenance-memory theory, some PF cells appear to buffer activity representing remembered information, even when distracting stimuli appear during the delay period (di Pellegrino and Wise 1993b; Miller et al. 1996; Moody et al. 1998). Although the interpretation of delay-period activity in terms of the short-term memory of a stimulus has a long history, many studies have explored alternatives.
Neurophysiological experiments designed to explore alternatives to the maintenance-memory interpretation of delay-period activity first attempted to dissociate sensory from motor signals. These studies showed that PFdl neurons preferentially reflected sensory signals, which supported the idea that these neurons encode stimulus memory over the short term. For example, one influential study used the “antisaccade” task (Funahashi et al. 1993b), in which a stimulus in one direction (from a central fixation point) instructed an eye movement in the opposite direction. More than twice as many PFdl neurons represented the location of the sensory stimulus as represented the target (or direction) of movement. In another experiment, when a given spatial cue guided two different reaching movements, motor factors affected PFdl neurons only rarely and weakly compared to neurons in the premotor cortex (di Pellegrino and Wise 1993b), especially when viewed at a population level (Wise et al. 1996a). These results supported the idea that more delay-period activity in PFdl reflected the memory of sensory cues than represented motor preparation or movement targets, but did not explore other alternative interpretations of delay-period activity.
Neuroimaging studies have provided support for some of these alternatives. At first, neuroimaging studies appeared to back the maintenance-memory theory of PF function, which bolstered the interpretation of PF's delay-period activity in the context of that theory. After an initial period of nearly uniform support, however, subsequent neuroimaging studies have suggested that PFdl plays a role in aspects of attention and other functions instead of, or in addition to, maintenance memory. Indeed, one recent report disputed whether PF plays any role in short-term memory at all. To quote the investigators, “no part of frontal cortex, including PF, stores mnemonic representation[s] . . . reliably across distracted delay periods. Rather, working memory storage . . . is mediated by a domain-specific network in posterior cortex” (Postle et al. 2003). Passingham and his colleagues have used the phrases attention to action, attention to intention, and attentional selection to describe certain PFdl functions (Rowe et al. 2000; Rowe and Passingham 2001). Petrides and his colleagues have, likewise, emphasized a role for PFdl in monitoring items in memory (Owen et al. 1996; Petrides et al. 2002). These alternative views of PF function point to a role in top-down control of attention and are supported by other neuroimaging and neuropsychological findings implicating PF in attentional functions (see Discussion).
In sum, then, neuroimaging and neuropsychological findings bring into question the interpretation of PFdl's delay-period activity mainly in terms of maintenance memory. Previous neurophysiological experiments have ruled out motor factors, such as motor planning and the representation of the targets of movement, for most of PFdl's delay-period activity, but have typically lacked control over spatial attention. The present experiment tested an alternative to the maintenance-memory interpretation of PFdl's delay-period activity by pitting the representation of a remembered location against the representation of an attended location, when either location could serve as the target of an upcoming saccadic eye movement.
[Emphases added by ISCID News Editor]
[Link-underlined terms with ^ indicate linked entry in ISCID Encyclopedia of Science and Philosophy as added by ISCID News Editor]
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[ 04. December 2004, 00:46: Message edited by: ISCID News Editor ]
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