Neural population dynamics underlying evidence accumulation in multiple rat brain regions

• Published in: eLife Vol. 13
• Main Authors: DePasquale, Brian, Brody, Carlos D, Pillow, Jonathan W
• Format: Journal Article
• Language: English
• Published: England eLife Sciences Publications Ltd 20.08.2024; eLife Sciences Publications, Ltd
• Subjects: Animals; Approximation; Behavior; Brain; Brain - physiology; Caudate-putamen; Choice Behavior; Cognitive ability; Computational and Systems Biology; Cortex (frontal); Cortex (parietal); Decision Making; evidence accumulation; latent variable models; Male; Models, Neurological; Neostriatum; Neurons; Neurons - physiology; Neuroscience; Parietal Lobe - physiology; Population dynamics; Rats; Standard deviation; computational biology; systems biology; evidence accumulation; rat; decision-making; neuroscience; latent variable models
• ISSN: 2050-084X; 2050-084X
• DOI: 10.7554/eLife.84955

Accumulating evidence to make decisions is a core cognitive function. Previous studies have tended to estimate accumulation using either neural or behavioral data alone. Here, we develop a unified framework for modeling stimulus-driven behavior and multi-neuron activity simultaneously. We applied our method to choices and neural recordings from three rat brain regions—the posterior parietal cortex (PPC), the frontal orienting fields (FOF), and the anterior-dorsal striatum (ADS)—while subjects performed a pulse-based accumulation task. Each region was best described by a distinct accumulation model, which all differed from the model that best described the animal’s choices. FOF activity was consistent with an accumulator where early evidence was favored while the ADS reflected near perfect accumulation. Neural responses within an accumulation framework unveiled a distinct association between each brain region and choice. Choices were better predicted from all regions using a comprehensive, accumulation-based framework and different brain regions were found to differentially reflect choice-related accumulation signals: FOF and ADS both reflected choice but ADS showed more instances of decision vacillation. Previous studies relating neural data to behaviorally inferred accumulation dynamics have implicitly assumed that individual brain regions reflect the whole-animal level accumulator. Our results suggest that different brain regions represent accumulated evidence in dramatically different ways and that accumulation at the whole-animal level may be constructed from a variety of neural-level accumulators.