Dataset Information

Differential roles of delay-period neural activity in the monkey dorsolateral prefrontal cortex in visual-haptic crossmodal working memory.

ABSTRACT: Previous studies have shown that neurons of monkey dorsolateral prefrontal cortex (DLPFC) integrate information across modalities and maintain it throughout the delay period of working-memory (WM) tasks. However, the mechanisms of this temporal integration in the DLPFC are still poorly understood. In the present study, to further elucidate the role of the DLPFC in crossmodal WM, we trained monkeys to perform visuo-haptic (VH) crossmodal and haptic-haptic (HH) unimodal WM tasks. The neuronal activity recorded in the DLPFC in the delay period of both tasks indicates that the early-delay differential activity probably is related to the encoding of sample information with different strengths depending on task modality, that the late-delay differential activity reflects the associated (modality-independent) action component of haptic choice in both tasks (that is, the anticipation of the behavioral choice and/or active recall and maintenance of sample information for subsequent action), and that the sustained whole-delay differential activity likely bridges and integrates the sensory and action components. In addition, the VH late-delay differential activity was significantly diminished when the haptic choice was not required. Taken together, the results show that, in addition to the whole-delay differential activity, DLPFC neurons also show early- and late-delay differential activities. These previously unidentified findings indicate that DLPFC is capable of (i) holding the coded sample information (e.g., visual or tactile information) in the early-delay activity, (ii) retrieving the abstract information (orientations) of the sample (whether the sample has been haptic or visual) and holding it in the late-delay activity, and (iii) preparing for behavioral choice acting on that abstract information.

SUBMITTER: Wang L

PROVIDER: S-EPMC4299181 | biostudies-literature | 2015 Jan

REPOSITORIES: biostudies-literature

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Differential roles of delay-period neural activity in the monkey dorsolateral prefrontal cortex in visual-haptic crossmodal working memory.

Wang Liping L Li Xianchun X Hsiao Steven S SS Lenz Fred A FA Bodner Mark M Zhou Yong-Di YD Fuster Joaquín M JM

Proceedings of the National Academy of Sciences of the United States of America 20141224 2

Previous studies have shown that neurons of monkey dorsolateral prefrontal cortex (DLPFC) integrate information across modalities and maintain it throughout the delay period of working-memory (WM) tasks. However, the mechanisms of this temporal integration in the DLPFC are still poorly understood. In the present study, to further elucidate the role of the DLPFC in crossmodal WM, we trained monkeys to perform visuo-haptic (VH) crossmodal and haptic-haptic (HH) unimodal WM tasks. The neuronal acti ...[more]

PMID: 25540412

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Project description:Exposure to cannabis impairs cognitive functions reliant on the circuitry of the dorsolateral prefrontal cortex (DLPFC) and increases the risk of schizophrenia. The actions of cannabis are mediated via the brain cannabinoid 1 receptor (CB1R), which in rodents is heavily localized to the axon terminals of cortical GABA basket neurons that contain cholecystokinin (CCK). Differences in the laminar distribution of CB1R-immunoreactive (IR) axons have been reported between rodent and monkey neocortex, suggesting that the cell type(s) containing CB1Rs, and the synaptic targets of CB1R-IR axon terminals, may differ across species; however, neither the relationship of CB1Rs to CCK-containing interneurons, nor the postsynaptic targets of CB1R and CCK axon terminals, have been examined in primate DLPFC. Consequently, we compared the distribution patterns of CB1R- and CCK-IR structures, determined the proportions of CB1R and CCK neurons that were dual-labeled, and identified the synaptic types and postsynaptic targets of CB1R- and CCK-IR axon terminals in macaque monkey DLPFC. By light microscopy, CB1R- and CCK-IR axons exhibited a similar laminar distribution, with their greatest densities in layer 4. Dual-label fluorescence experiments demonstrated that 91% of CB1R-IR neurons were immunopositive for CCK, whereas only 51% of CCK-IR neurons were immunopositive for CB1R. By electron microscopy, all synapses formed by CB1R-IR axon terminals were symmetric, whereas CCK-IR axon terminals formed both symmetric (88%) and asymmetric (12%) synapses. The primary postsynaptic target of both CB1R- and CCK-IR axon terminals forming symmetric synapses was dendritic shafts (81-88%), with the remainder targeting cell bodies or dendritic spines. Thus, despite species differences in laminar distribution, CB1Rs are principally localized to CCK basket neuron axons in both rodent neocortex and monkey DLPFC. These axons target the perisomatic region of pyramidal neurons, providing a potential anatomical substrate for the impaired function of the DLPFC associated with cannabis use and schizophrenia.

Dataset Information

Differential roles of delay-period neural activity in the monkey dorsolateral prefrontal cortex in visual-haptic crossmodal working memory.

Publications

Differential roles of delay-period neural activity in the monkey dorsolateral prefrontal cortex in visual-haptic crossmodal working memory.

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