Parallel processing, hierarchical transformations, and sensorimotor associations along the ‘where’ pathway

Abstract

Visually guided behaviors require the brain to transform ambiguous retinal images into object-level spatial representations and implement sensorimotor transformations. These processes are supported by the dorsal 'where' pathway. However, the specific functional contributions of areas along this pathway remain elusive due in part to methodological differences across studies. We previously showed that macaque caudal intraparietal (CIP) area neurons possess robust three-dimensional (3D) visual representations, carry choice- and saccade-related activity, and exhibit experience-dependent sensorimotor associations (Chang et al., 2020b). Here, we used a common experimental design to reveal parallel processing, hierarchical transformations, and the formation of sensorimotor associations along the 'where' pathway by extending the investigation to V3A, a major feedforward input to CIP. Higher-level 3D representations and choice-related activity were more prevalent in CIP than V3A. Both areas contained saccade-related activity that predicted the direction/timing of eye movements. Intriguingly, the time-course of saccade-related activity in CIP aligned with the temporally integrated V3A output. Sensorimotor associations between 3D orientation and saccade direction preferences were stronger in CIP than V3A, and moderated by choice signals in both areas. Together, the results explicate parallel representations, hierarchical transformations, and functional associations of visual and saccade-related signals at a key juncture in the 'where' pathway.

Hierarchical computation of 3D motion across macaque areas MT and FST

“…Most importantly, the significance of the main effect of motion direction did not depend on whether vergence was included as a covariate for all but 4 (2.1%) MT and 3 (1.0%) FST neurons. These findings are similar to those in previous reports 8 , 14 , 29 , 34 , 64 , 75 and imply that vergence signals did not account for 3D motion selectivity.…”

“… 68 Tetrode-based spike sorting was performed offline using the KlustaKwik 69 semi-automatic clustering algorithm in MClust 4.0 70 followed by manual refinement based on waveform, stability, and refractory period violations in Offline Sorter (Plexon, Inc). As in previous work, 34 , 64 all isolated units were verified by at least two authors. Only neurons for which the stimulus was entirely within the RF were included: 193 MT and 317 FST neurons from the right hemisphere of Monkey J (33 MT and 33 FST sessions); 165 MT and 217 FST neurons from the left hemisphere of Monkey C (12 MT and 20 FST sessions).…”

“…A head-stabilizing Delrin ring was surgically attached to the skull under general anesthesia. 29 , 34 , 61 – 64 After recovery, the monkeys were trained to sit in a primate chair and fixate visual targets within 2° version and 1° vergence windows for liquid reward. Both monkeys previously participated in a study which used the same stimuli and discrimination task to assess behavioral sensitivity to perspective and stereoscopic cues to 3D motion across the visual field.…”

“…The spike times of individual neurons were aligned to the stimulus onset using the phototransistor trace. Following previous work, 34 , 64 spikes were binned with 1 ms resolution and convolved with a double exponential function, which was averaged over all trials to generate an average spike density function (SDF). The response latency was then defined as the first time point after stimulus onset when the SDF significantly deviated from the average level of baseline activity (computed over all trials using the 150 ms of fixation preceding the stimulus onsets) with maintained significance for at least 30 ms (ANOVA followed by Tukey’s HSD test, p < 0.05).…”

Deriving connectivity from spiking activity in biophysical cortical microcircuits

“…More complex perturbation protocols could include modeling a variety of sensory stimulus presentations e.g. using different orientations 44,51 or motion tasks 52,53 to activate different subgroups of neurons at a time.…”