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      Sharp emergence of feature-selective sustained activity along the dorsal visual pathway

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      Nature neuroscience

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          Abstract

          Sustained activity encoding visual working memory representations has been observed in several cortical areas of primates. Where along the visual pathways this activity emerges remains unknown. Here we show in macaques that sustained spiking activity encoding memorized visual motion directions is absent in direction-selective neurons in early visual area middle temporal (MT). However, it is robustly present immediately downstream, in multimodal association area medial superior temporal (MST), and in the lateral prefrontal cortex (LPFC). This sharp emergence of sustained activity along the dorsal pathway suggests a functional boundary between early visual areas, encoding sensory inputs, and downstream association areas, additionally encoding mnemonic representations. Moreover, local field potential oscillations in MT encoded the memorized directions and, in the low frequencies, were phase-coherent with LPFC spikes. This suggests that LPFC sustained activity modulates synaptic activity in MT, a putative top-down mechanism by which memory signals influence stimulus processing in early visual cortex.

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          Most cited references45

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          Working Memory: Theories, Models, and Controversies

          I present an account of the origins and development of the multicomponent approach to working memory, making a distinction between the overall theoretical framework, which has remained relatively stable, and the attempts to build more specific models within this framework. I follow this with a brief discussion of alternative models and their relationship to the framework. I conclude with speculations on further developments and a comment on the value of attempting to apply models and theories beyond the laboratory studies on which they are typically based.
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            Cellular basis of working memory

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              Mnemonic coding of visual space in the monkey's dorsolateral prefrontal cortex.

              1. An oculomotor delayed-response task was used to examine the spatial memory functions of neurons in primate prefrontal cortex. Monkeys were trained to fixate a central spot during a brief presentation (0.5 s) of a peripheral cue and throughout a subsequent delay period (1-6 s), and then, upon the extinction of the fixation target, to make a saccadic eye movement to where the cue had been presented. Cues were usually presented in one of eight different locations separated by 45 degrees. This task thus requires monkeys to direct their gaze to the location of a remembered visual cue, controls the retinal coordinates of the visual cues, controls the monkey's oculomotor behavior during the delay period, and also allows precise measurement of the timing and direction of the relevant behavioral responses. 2. Recordings were obtained from 288 neurons in the prefrontal cortex within and surrounding the principal sulcus (PS) while monkeys performed this task. An additional 31 neurons in the frontal eye fields (FEF) region within and near the anterior bank of the arcuate sulcus were also studied. 3. Of the 288 PS neurons, 170 exhibited task-related activity during at least one phase of this task and, of these, 87 showed significant excitation or inhibition of activity during the delay period relative to activity during the intertrial interval. 4. Delay period activity was classified as directional for 79% of these 87 neurons in that significant responses only occurred following cues located over a certain range of visual field directions and were weak or absent for other cue directions. The remaining 21% were omnidirectional, i.e., showed comparable delay period activity for all visual field locations tested. Directional preferences, or lack thereof, were maintained across different delay intervals (1-6 s). 5. For 50 of the 87 PS neurons, activity during the delay period was significantly elevated above the neuron's spontaneous rate for at least one cue location; for the remaining 37 neurons only inhibitory delay period activity was seen. Nearly all (92%) neurons with excitatory delay period activity were directional and few (8%) were omnidirectional. Most (62%) neurons with purely inhibitory delay period activity were directional, but a substantial minority (38%) was omnidirectional. 6. Fifteen of the neurons with excitatory directional delay period activity also had significant inhibitory delay period activity for other cue directions. These inhibitory responses were usually strongest for, or centered about, cue directions roughly opposite those optimal for excitatory responses.(ABSTRACT TRUNCATED AT 400 WORDS)
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                Author and article information

                Journal
                9809671
                21092
                Nat Neurosci
                Nat. Neurosci.
                Nature neuroscience
                1097-6256
                1546-1726
                3 August 2016
                10 August 2014
                September 2014
                09 August 2016
                : 17
                : 9
                : 1255-1262
                Affiliations
                Cognitive Neurophysiology Laboratory, Department of Physiology, McGill University, Montreal, Canada
                Article
                CAMS4573
                10.1038/nn.3785
                4978542
                25108910
                30dab6c1-2bb2-4165-b2a4-829a54b7ab7e

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                Neurosciences

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