Choice activity stabilizes sensory representations and mediates sensorimotor associations in parietal cortex

Abstract

33Selecting actions which achieve desired goals often requires three-dimensional (3D) 34representations of the environment. Because the sensory epithelia cannot directly encode the 35 world's 3D spatial features, sensory signals must be converted into 3D representations. Here we 36 investigated the relationships between the quality of 3D visual representations, choice-related 37 activity, and motor-related activity in the parietal cortex of macaque monkeys using an eight-38 alternative 3D orientation discrimination task, visually guided saccade task, and laminar probe 39 recordings. We found that choice activity was preferentially carried by caudal intraparietal area 40 neurons with more robust 3D representations. Choice activity further stabilized the 3D 41representations, rather than attenuating information not directly relevant to the behavioral task 42 (nuisance variables). An experience-dependent, sensorimotor association additionally aligned 43 sensory and saccade direction preferences, particularly for neurons with choice activity. These 44 findings reveal novel roles for choice activity in improving the fidelity of ecologically relevant object 45 representations and mediating sensorimotor associations. 46 (Tsutsui et al., 2001;Van Dromme et al., 2016). 67 47The anatomical projections and effective connectivity of CIP suggest that it may also 68 contribute to goal-directed sensorimotor transformations (Nakamura et al., 2001; Premereur et 69 al., 2015;Van Dromme et al., 2016; Lanzilotto et al., 2019). In particular, CIP projects to areas 70 involved in motor planning and execution, including the lateral intraparietal area (LIP) (Andersen 71 et al., 1992;Bennur and Gold, 2011;Shushruth et al., 2018), anterior intraparietal area (Murata 72 et al., 2000;Baumann et al., 2009;Pani et al., 2014), and V6A (Fattori et al., 2010; Fattori et al., 73 2012;Breveglieri et al., 2016). However, it is untested if CIP carries motor-related signals, or if its 74 output only contains 3D sensory information. 75Here we investigated the relationships between sensory representations, choice-related 76 activity, and motor-related activity in CIP. Neuronal activity was recorded while macaque monkeys 77 performed an eight-alternative forced choice (8AFC) tilt discrimination task with planar surfaces 78 presented at different slants and distances . The neurons differed in the extent 79 to which their 3D orientation selectivity depended on distance. Choice activity was preferentially 80 carried by neurons with more robust 3D representations, and further stabilized 3D selectivity. 81Choice tuning was parametric, and the choice and tilt preferences aligned. Motor-related activity 82 was assessed using a visually guided saccade task (Munoz and Wurtz, 1995; Hanes and Schall, 83 1996). We found that many CIP neurons had saccade direction tuning. Moreover, the surface tilt 84 and saccade direction preferences were mapped onto one another, reflecting a sensorimotor 85 association that was strongest for neurons with choice acti...