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

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.

Correlated variability modifies working memory fidelity in primate prefrontal neuronal ensembles

“…Previous studies have decoded the identity of stimuli maintained in spatial (39,40) and nonspatial WM (8,39) in pseudopopulations of LPFC neurons, typically using sets of 2 to 8 unique stimuli. We were able to reliably decode which of 16 target locations was being held in WM during the delay epoch by applying a linear support vector machine (SVM) (Materials and Methods) to simultaneously recorded ensemble data ( Fig.…”

“…Fuster and Alexander later discovered neurons in the lateral prefrontal cortex (LPFC) of monkeys that exhibited sustained firing during WM tasks (4). Subsequent neurophysiological studies have corroborated that neuronal activity in the LPFC and other regions can represent WM for visual-mnemonic space (5-7), as well as nonspatial visual features (8)(9)(10).…”

Simultaneous representation of sensory and mnemonic information in human visual cortex

“…On the other hand, a mismatch test stimulus would drive a new set of neurons, which may lead to a lower overall response due to inhibitory competition with the already active neurons tuned to the sample feature (Serences, 2016;Gayet, et al, 2017). The same logic also applies if the top-down modulations supporting VWM do not lead to sustained patterns of spiking in sensory cortices, and instead only influence sub-threshold potentials (Mendoza-Halliday, Torres, & Martinez-Trujillo, 2014;Merrikhi et al, 2017). Differences in the local comparison circuit output would still be expected due to interactions between the top-down feature-selective bias and the sensory response evoked by the test stimulus.…”

“…Thus, a delay period devoid of other visual inputs is quite divorced from typical visual experience. Based on this mismatch between experimental and real-world scenarios, some have argued that recruiting early sensory areas to store relevant VWM information would be counterproductive in everyday life, as new sensory inputs would destructively interfere with concurrent mnemonic representations (Bettencourt & Xu, 2016;Mendoza-Halliday, Torres, & Martinez-Trujillo, 2014;Stokes, 2015).…”

Transitions between Multiband Oscillatory Patterns Characterize Memory-Guided Perceptual Decisions in Prefrontal Circuits

“…It is implicated in spatial working memory (Funahashi et al, 1989) and in selective attention, providing topdown signals to other cortical areas (Moore and Armstrong, 2003;Buschman and Miller, 2007;Salazar et al, 2012;Gregoriou et al, 2014;Mendoza-Halliday et al, 2014;Womelsdorf et al, 2014;Siegel et al, 2015). To carry out these cognitive functions, the PFC has to participate in a variety of computational processes, including the handling of current sensory inputs, the selection and retention of relevant information, and the modulatory control of other brain areas.…”