Distinct fMRI Responses to Self-Induced versus Stimulus Motion during Free Viewing in the Macaque

Abstract

Visual motion responses in the brain are shaped by two distinct sources: the physical movement of objects in the environment and motion resulting from one's own actions. The latter source, termed visual reafference, stems from movements of the head and body, and in primates from the frequent saccadic eye movements that mark natural vision. To study the relative contribution of reafferent and stimulus motion during natural vision, we measured fMRI activity in the brains of two macaques as they freely viewed Ͼ50 hours of naturalistic video footage depicting dynamic social interactions. We used eye movements obtained during scanning to estimate the level of reafferent retinal motion at each moment in time. We also estimated the net stimulus motion by analyzing the video content during the same time periods. Mapping the responses to these distinct sources of retinal motion, we found a striking dissociation in the distribution of visual responses throughout the brain. Reafferent motion drove fMRI activity in the early retinotopic areas V1, V2, V3, and V4, particularly in their central visual field representations, as well as lateral aspects of the caudal inferotemporal cortex (area TEO). However, stimulus motion dominated fMRI responses in the superior temporal sulcus, including areas MT, MST, and FST as well as more rostral areas. We discuss this pronounced separation of motion processing in the context of natural vision, saccadic suppression, and the brain's utilization of corollary discharge signals.

Functional Subpopulations of Neurons in a Macaque Face Patch Revealed by Single-Unit fMRI Mapping

“…To investigate the moment-to-moment brain activity that is not strictly driven by repeated presentations of a stimulus, it is necessary to collect measures of interest in parallel. For example, in a previous study, we analyzed fMRI data with respect to the moment-by-moment eye gaze behavior (Russ et al 2016). Extending this type of approach to the relationship between single units and fMRI requires simultaneous recordings in the fMRI scanner, which is now readily achievable (Godlove et al, Society for Neuroscience Annual Meeting Abstr., 2015).…”

“…That study presented both flashed images and natural videos and, like other recent work (Bartels and Zeki, 2005; Hasson et al, 2010; Hasson et al, 2004; Huth et al, 2012; Russ et al, 2016; Russ and Leopold, 2015; Sheinberg and Logothetis, 2001), focused on the brain’s processing of naturalistic and dynamic stimuli during free viewing. Critically, that study relied upon chronic microwire bundles to sample neurons within a few hundred microns of one another and to record a large number of responses from the same neurons over weeks at a time.…”

Neurons in primate prefrontal cortex signal valuable social information during natural viewing

“…The use of naturalistic video stimuli to expose non-human primates to a visual context with increased external validity has been invaluable for improving our understanding of both natural vision (e.g. [ 45 ]) and social cognition (e.g. [ 46 ]).…”

atlasBREX: Automated template-derived brain extraction in animal MRI

“…In recent years, neuroimaging studies with animal models, such as macaque 2 , marmoset 3,4 and rodent 5 , gained in significance due to their contributions to understanding the central nervous system 6,7 . To date, however, there are only few technical approaches available that can be applied to animal MRI, such as Marker based watershed scalper (MBWSS) 8 , Brain-Extraction-Tool (BET) 9 , 3dSkullStrip (3DSS) as part of the Analysis of Functional NeuroImages (AFNI) package 10 , Primatologist-Toolbox (PRIMA) 11 , Rapid Automatic Tissue Segmentation (RATS) 12 and Robust automatic rodent brain extraction using 3D pulse-coupled neural networks (PCNN3D) 13 .…”