Multitasking of Attention and Memory Functions in the Primate Prefrontal Cortex

Abstract

In motor and sensory areas of cortex, neuronal activity often depends on the location of a movement target or a sensory stimulus, with each neuron tuned to a single part of space called a preferred direction (when motor) or a receptive field (when sensory). As we previously reported, some neurons in the monkey prefrontal cortex are tuned to two parts of space, which we interpreted as reflecting attention and working memory, respectively. Monkeys performed a behavioral task in which they attended to a visual stimulus at one location while remembering a second place, and these locations were varied from trial to trial to assess spatial tuning. Most spatially tuned neurons specialized in either attentional or mnemonic processing, but about one-third of the cells showed tuning for both. Here, we show that the latter population, called multitasking neurons, improves the encoding of both the attended and remembered locations. These neurons do so for three reasons: (1) the preferred directions for attention and for working memory usually differ (and often diametrically oppose one another), (2) they have stronger tuning than specialized cells, and (3) pairs of multitasking neurons represent these cognitive parameters more efficiently than pairs that include even a single specialized cell. These findings suggest that multitasking neurons provide a computational advantage for behaviors that place simultaneous demands on two or more cognitive processes.

Saccade Planning Evokes Topographically Specific Activity in the Dorsal and Ventral Streams

“…We used two independent saccade conditions that allowed us to measure the effects of covert attention and saccade planning at separate retinal locations. A similar logic was used to dissociate spatial attention and saccade preparation in FEF (Juan et al, 2004), and memory and attention in dorsolateral prefrontal cortex (Messinger et al, 2009). We found early transient responses time-locked to the presentation of the saccade target in both prosaccade and antisaccade trials that mapped to the retinotopic location of the attended visual target, consistent with previous studies of the effects of attention on visual cortex (Pestilli et al, 2011).…”

“…Perhaps the nature of the top-down signal could be causing the inconsistent results; brief microstimulation might not evoke as large of a BOLD response as long epochs of saccade preparation. In aggregate, it appears as if spatially specific topdown signals caused by saccade planning, attention, and working memory may each effect activity in early visual cortex similarly, despite that these spatial cognitive abilities may have distinct neuronal origins (Juan et al, 2004;Messinger et al, 2009;Suzuki and Gottlieb, 2013). Future work should target whether these effects and their functional consequences are dissociable at the level of the visual cortex.…”

Multiple component networks support working memory in prefrontal cortex

“…In some cases, spatial WM may depend on the sustained allocation of attention to the spatial location of the memorized cue (29,30). Although human fMRI studies disagree on whether attention mechanisms account for activity in PFC during WM maintenance (30,31), at the cellular level, neurons in monkey PFC can encode stored locations and attended locations, and some even encode both (32). Although our study was not designed to distinguish between the storage and attention-related cognitive mechanisms, it firmly establishes a mode of population activity in PFC that encodes locations only when visual cues have been extinguished during the memory delay.…”

Primate models of interference control

“…Lebedev et al [30] Monkey memory-guided saccade + luminance discrimination Messinger et al [31 ] Monkey memory-guided saccade + luminance discrimination Miyazaki et al [32] Monkey memory-guided + visually-guided bimanual motor task. Watanabe and Funahashi [33 ] Monkey DMP + spatial attention task a DMS: delayed matching-to-sample task.…”

“…In the monkey's lateral prefrontal cortex (LPFC), Wise and colleagues [30,31 ] examined the neural mechanisms related to interference effects using a dual-task-like paradigm (Figure 2a). In their task, while…”