Elsevier

NeuroImage

Volume 109, 1 April 2015, Pages 84-94
NeuroImage

Functional MRI mapping of dynamic visual features during natural viewing in the macaque

https://doi.org/10.1016/j.neuroimage.2015.01.012Get rights and content

Highlights

  • We used a natural viewing paradigm to generate fMRI feature maps.

  • We were able to map face patches with as little as 15 min of natural viewing.

  • Motion dominated fMRI responses throughout the ventral visual pathway.

  • Motion contributed much less to fMRI responses to videos without social content.

Abstract

The ventral visual pathway of the primate brain is specialized to respond to stimuli in certain categories, such as the well-studied face selective patches in the macaque inferotemporal cortex. To what extent does response selectivity determined using brief presentations of isolated stimuli predict activity during the free viewing of a natural, dynamic scene, where features are superimposed in space and time? To approach this question, we obtained fMRI activity from the brains of three macaques viewing extended video clips containing a range of social and nonsocial content and compared the fMRI time courses to a family of feature models derived from the movie content. Starting with more than two dozen feature models extracted from each movie, we created functional maps based on features whose time courses were nearly orthogonal, focusing primarily on faces, motion content, and contrast level. Activity mapping using the face feature model readily yielded functional regions closely resembling face patches obtained using a block design in the same animals. Overall, the motion feature model dominated responses in nearly all visually driven areas, including the face patches as well as ventral visual areas V4, TEO, and TE. Control experiments presenting dynamic movies, whose content was free of animals, demonstrated that biological movement critically contributed to the predominance of motion in fMRI responses. These results highlight the value of natural viewing paradigms for studying the brain's functional organization and also underscore the paramount contribution of magnocellular input to the ventral visual pathway during natural vision.

Introduction

During an animal's natural visual experience, the brain receives information about the environment in a manner that differs from that in most electrophysiological or fMRI experiments. For example, when a macaque monkey observes its conspecifics, visual input consists not of a series of isolated presentations, but of an evolving thread of dynamic, high- and low-level features superimposed in space and time. While it is straightforward to record neural or fMRI activity while monkeys observe natural movies, few such experiments have been carried out, likely because of the challenges inherent in the data analysis and interpretation. However, given that the brain evolved and operates under such conditions, it may be of great value to use natural paradigms that can complement more conventional approaches to assess functional responses in the brain.

Human fMRI experiments have begun to develop and apply such paradigms, often by having subjects watch commercial movies. Various experiments have used voxel time courses to assess the shared signal variation across brain areas (Bartels and Zeki, 2004, Bartels and Zeki, 2005), map intersubject correlations (Hasson et al., 2004, Hasson et al., 2008), and measure the degree to which brain activity is predicted by certain features (Bartels et al., 2008, Hanson et al., 2007, Huth et al., 2012). These studies have shown that, despite the challenges of superimposed features, it is possible to create functional maps and assess aspects of functional brain organization under natural viewing conditions. One study has gone further, matching the voxel time courses in the human brain to those in macaques watching the same movies with the aim of establishing homological correspondence between the species (Mantini et al., 2012, Mantini et al., 2013).

The macaque extrastriate visual cortex is characterized by having a large number of specialized areas. Visual signals are analyzed by regions apparently dedicated for the processing of motion (Maunsell and Van Essen, 1983), complex spatial structure (Fujita et al., 1992), and spatial cues (Andersen, 1985). Testing with fMRI has identified functional networks, such as that specialized for the processing of faces (Tsao et al., 2003). Does this apparent division of labor, derived from conventional testing, govern neural activity in the macaque's brain during natural viewing?

Here we explore this question by measuring fMRI activity in macaques freely viewing extended natural videos containing diverse social and nonsocial content. Using a family of feature models extracted from each video, we assessed the relative contribution of different visual features throughout the brain. We first show that face feature models yield maps that bear striking similarity to the face patches identified using conventional block design. We next show that in the face patches, as well as in neighboring regions of V4, TEO and TE, the motion feature models, whose time courses are largely uncorrelated with the face feature models, are the primary drivers of the fMRI voxel time courses. These findings demonstrate that natural viewing paradigms can be valuable assays of functional specialization in the macaque brain, and additionally underscore the strong contribution of magnocellular input to ventral stream visual processing during natural vision.

Section snippets

Subjects

Three adult female rhesus monkeys (M1, M2, M3) participated in the study. Prior to training, monkeys were implanted with a custom-designed and fabricated fiberglass headpost, which was used to immobilize the head during testing. All procedures were approved by the Animal Care and Use Committee of the US National Institutes of Health (National Institute of Mental Health) and followed US National Institutes of Health guidelines. Surgery was performed using sterile procedures (see Maier et al.,2008

Results

The main goal of the study was to measure the contribution of different stimulus features to fMRI responses throughout the brain during natural viewing. The fMRI data were obtained from three monkeys, who repeatedly viewed up to eighteen 5-min natural videos inside the bore of a 4.7 T vertical scanner. The movies varied in their content, but generally depicted conspecific and heterospecific monkeys, humans, and other animals engaged in a variety of social and nonsocial behaviors (see Video S1

Discussion

We used fMRI data collected during the free viewing of natural movies to investigate how the brain processes visual features that co-occur during natural vision. We found that we could readily map the locations of the face patches across three animals using a model based on the presence of faces. Additionally, we found that motion dominated the responses throughout the ventral visual stream, both within known motion selective regions in the lower bank of the STS (Bartels et al., 2008, Fischer

Acknowledgments

We would like to thank Tahir Haque for scoring the videos, Charles Zhu and Dr. Frank Ye for assistance with fMRI scanning, Katy Smith, George Dold and David Ide for excellent technical assistance and development, Drs. Takaaki Kaneko and Saleem Kadharbatcha for helpful discussion, Hang Joon Jo, Ziad Saad and Colin Reveley for guidance in fMRI analysis, and Drs. Chia-chun Hung and Brian Scott for comments on the manuscript. Functional and anatomical MRI scanning was carried out in the

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