Abstract
Comparing sequential stimuli is crucial for guiding complex behaviors. To understand mechanisms underlying sequential decisions, we compared neuronal responses in the prefrontal cortex (PFC), the lateral intraparietal (LIP), and medial intraparietal (MIP) areas in monkeys trained to decide whether sequentially presented stimuli were from matching (M) or nonmatching (NM) categories. We found that PFC leads M/NM decisions, whereas LIP and MIP appear more involved in stimulus evaluation and motor planning, respectively. Compared to LIP, PFC showed greater nonlinear integration of currently visible and remembered stimuli, which correlated with the monkeys' M/NM decisions. Furthermore, multi-module recurrent networks trained on the same task exhibited key features of PFC and LIP encoding, including nonlinear integration in the PFC-like module, which was causally involved in the networks' decisions. Network analysis found that nonlinear units have stronger and more widespread connections with input, output, and within-area units, indicating putative circuit-level mechanisms for sequential decisions.
Highlights
The ability to compare and make decisions about sequentially presented sensory stimuli is essential for generating appropriate behavioral responses to the stimuli and events in our surroundings
Higher error rates were observed on match compared to non-match trials for all three data sets of both monkeys (Supplementary table 1). These results indicate that monkeys reliably based their M/NM decisions on the category membership of both sample and test stimuli
The activity of match-preferring neurons in MIP during both match and non-match trials was very similar both before and during the hand movement (200-0 ms prior to the hand movement, Figure 4C, p = 0.99, paired t-test). These results suggest that match-preferring neurons in prefrontal cortex (PFC) and LIP are more involved in nonmotor functions during M/NM decisions, such as the comparison of sample and test categories, while match-preferring neurons in MIP are primarily involved in motor functions such as planning and/or initiating hand/arm movements
Summary
The ability to compare and make decisions about sequentially presented sensory stimuli is essential for generating appropriate behavioral responses to the stimuli and events in our surroundings. Such sequential decisions require incoming sensory information to be compared to information maintained in short-term memory. LIP and MIP are often associated with visuospatial processing related to attention and movement planning (Andersen and Buneo, 2002; Andersen et al, 1997; Bisley and Goldberg, 2003, 2010; Colby and Goldberg, 1999; Cui and Andersen, 2007; Gnadt and Andersen, 1988; Gottlieb et al, 1998; Malhotra et al, 2009; Snyder et al, 1997; Zhou et al, 2016), as well as more cognitive functions such as perceptual decisions (Hanks et al, 2006; Huk and Shadlen, 2005; Kiani and Shadlen, 2009; Platt and Glimcher, 1999; Roitman and Shadlen, 2002; Shadlen and Newsome, 1996; Yang and Shadlen, 2007; Zhou and Freedman, 2019)
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