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.prefrontal | cross-modal working memory | monkey | delay activity | single unit W orking memory (WM) is a central concept in cognitive sciences. The prefrontal cortex constitutes the highest stage in the cortical hierarchy of executive memories (1-5), and it seems to be essential for integrating sensory information of different modalities with subsequent action in goal-directed behavior (6-9).Cells involved in WM ("memory cells") were first recorded in the dorsolateral prefrontal cortex (DLPFC) of monkeys performing delayed-response tasks (10-12) and have also been reported by other subsequent primate studies (13-19). The persistent delay activity recorded in those studies reflects the maintenance of a working-memory representation and therefore underlies the representation of retrospective, current, and prospective information (20). From the results of those studies, it seems that, in addition to persistent delay activity that is sustained throughout the whole delay period in WM tasks, task/set cells, eye movement-related responses, and phasic sensory responses, etc. (14-18, 21), two other general types of prefrontal neurons have also been studied (22, 23). One is the so-called sensory-coupled cue cell, the discharge of wh...

Stable Delay Period Representations in the Posterior Parietal Cortex Facilitate Working-Memory-Guided Obstacle Negotiation

“…Similarly, in previous WM studies, early delay period modulation has been attributed to the encoding of task-relevant information in macaque prefrontal neurons [14,15,25,26]. In addition to such ''sensory-coupled cue cells,'' previous studies also describe a separate group of ''preparatory set cells,'' which increase their activity throughout a WM delay [26]. This late-delay modulation is often attuned to the WM-guided action following the delay, such as the direction of a saccade [42] or manual response [25], and can be exhibited as a ''ramping'' of neural activity toward the end of a fixed delay [43].…”

“…As such, delay period modulation related to foreleg obstacle clearance, especially during the early delay, may encode this information into WM in order to guide the hindlegs over the same obstacle following the delay. Similarly, in previous WM studies, early delay period modulation has been attributed to the encoding of task-relevant information in macaque prefrontal neurons [14,15,25,26]. In addition to such ''sensory-coupled cue cells,'' previous studies also describe a separate group of ''preparatory set cells,'' which increase their activity throughout a WM delay [26].…”

“…In addition to sustained activation persisting throughout a WM delay, recent studies of WM-guided behaviors have reported phasic delay period activation [25,26]. Modulated activity peaking early during a WM delay is presumed to represent sensory encoding of task-relevant information, and modulated activity peaking later in the delay is thought to be motor related and important for preparing the upcoming action.…”

“…Such phasic, rather than persistent, modulation occurring momentarily throughout a delay may be important for information encoding and movement planning in WM tasks [25,26].…”

Overview of Prefrontal Functions

“…Supporting this assertion are unit data from the primate cortex showing that the cells that participate in working memory belong to widely distributed networks attuned to multiple associated features of the memorandum, even if these features pertain to different sensory modalities (Fuster et al, 2000;Zhou et al, 2007;Mante et al, 2013;Wang et al, 2015). One is its associative character.…”