A rapid fMRI task battery for mapping of visual, motor, cognitive, and emotional function

doi:10.1016/j.neuroimage.2005.12.016

NeuroImage

Volume 31, Issue 2, June 2006, Pages 732-744

https://doi.org/10.1016/j.neuroimage.2005.12.016 Get rights and content

Abstract

A set of sensory, motor, cognitive, and emotional tasks were combined in a simple, rapid-presentation task battery and tested on a group of 31, normal, healthy subjects aged 22 to 76. Five tasks were selected on the basis of widespread use in fMRI and their ability to produce robust and reliable regional activations. They were (1) a visual task designed to activate the occipital cortex; (2) a bimanual motor task designed to activate motor areas; (3) a verb generation task designed to activate speech processing areas; (4) an n-back task designed to activate areas associated with working memory and executive function; and (5) an emotional pictures task designed to provoke strong emotional responses that typically activate limbic structures. Most of the tasks produced reliable activations in individual subjects, and assessments of the distribution and reliability of individual subject activations in each targeted area are provided. The emotional pictures task did not demonstrate adequate sensitivity in a priori target regions, only in the a posteriori defined inferior temporal region. Age- and gender-specific differences were found in the activation patterns for both the cognitive and emotional tasks. The battery provides a prescribed means for researchers to obtain reliable functional localizers within 20–25 min of scanning, which can be used to support more elaborate mapping studies of brain function. The dataset can also serve as a reliability metric for new fMRI laboratories and novice investigators seeking to test their acquisition and analysis techniques with minimal time investment and expense.

Introduction

Many studies have demonstrated that functional magnetic resonance imaging (fMRI) can reliably activate specific sensory, cognitive, and limbic systems within the human brain (Moonen and Bandettini, 1999, Cabeza and Nyberg, 2000, Cabeza and Kingstone, 2001, Sabatinelli et al., 2005). Most fMRI studies concentrate on one specific functional system and devote entire scanning sessions to probing its behavior. There are, however, numerous circumstances in which it would be advantageous to collect data from multiple systems within the brain of a single subject. While the time and expense associated with repeated fMRI sessions often discourages such studies, the development of a rapid and reliable task battery that targets multiple systems and can be performed in one study session could be put to use in a wide range of functional imaging applications. These include, for example, the localization of “eloquent” speech areas for neurosurgical planning, the establishment of functional activation markers for use in probing more complex regional functions, use as a benchmark dataset for testing in new imaging laboratories, and deployment as an educational tool for fMRI training. Accordingly, the principle goal of the present work is to demonstrate the viability of acquiring stable and reliable data from multiple brain systems with minimal commitment of scanner time. In the present study, we developed a battery of tasks that provides markers of activity in multiple brain systems (i.e., sensory, motor, cognitive, and limbic) in individual subjects within a relatively short acquisition time of 2.5 min per task or approximately 12.5 min for one run of the full functional battery (apart from the anatomical acquisition).

In clinical practice, several paradigms are used to identify the sensory and motor areas (Lee et al., 1998, Bittar et al., 1999, Boling et al., 1999) and language-related areas (Binder et al., 1997, FitzGerald et al., 1997, Benson et al., 1999, Fernandez et al., 2001). Some batteries have been developed for neurosurgical planning that include multiple, overlapping tasks for motor and language mapping (Tomczak et al., 2000, Heilbrun et al., 2001, Haberg et al., 2004), and one battery includes tasks for motor, sensory, and language mapping (Hirsch et al., 2000). These batteries target regions considered most critical for surgical decisions and are designed for patients with a wide range of symptoms and abilities. Consequently, the clinical batteries are designed to be simple to perform, so that the largest number of potentially impaired patients might comply with task directions, and they are geared to be most sensitive in visual, motor, and language areas that surgeons wish to spare to avoid devastating handicaps to patients. Such batteries consequently tend to ignore mapping of limbic and non-language cognitive functions.

The goals of this study were to develop a suite of common behavioral tasks, targeting sensory–motor areas as well as more complex cognitive and emotional functions, and that (a) can reliably localize the visual, motor, language, working memory, and limbic systems in individual subjects; (b) requires minimal data acquisition time to produce statistically reliable activity within predicted brain areas; (c) can be reproduced in any imaging center with standard functional imaging capabilities and basic analysis tools; and (d) can be used to produce functional localizers to support cross-laboratory comparisons. While the majority of data reported from fMRI tests are obtained on a relatively young cross-section of the population, mostly college students in their twenties, the present battery was tested on a cohort of subjects with a wider range of ages and educational and cultural backgrounds, thereby providing for an examination of age-based differences and allowing the results to be generalized to a broader population base. Other factors – such as head motion, task performance, and subject compliance – were evaluated to assess their impact on the ability of the task battery to accurately localize brain activity.

Section snippets

Subjects

Thirty-one, normal, healthy adults from age 22 to 76 (mean age 41 ± 15.3) were recruited for the study. All subjects were right-handed and fluent in English, with 25 native English speakers. Approximately an equal number of subjects were recruited to form three age groups: those age 30 or less, those 31 to 50 years old, and those older than 50. The youngest group of subjects was composed primarily of undergraduate and graduate students, thus providing a basis of comparison with the most common

Subject compliance, head movement, and task performance

Data regarding subject compliance, head movement, and performance are summarized in Table 1. The a priori inclusion criteria required performance with greater than 70% accuracy on each task and overall head motion of less than 1 voxel in size in any direction. All subjects, even those in the oldest group, were able to adequately hold their heads still and perform the tasks in the battery, so all subjects contributed data to the analyses. However, one run from a subject in the youngest group and

Discussion

A set of “classical” sensory–motor, cognitive, and emotional tasks was combined in a task battery and tested on a group of normal, healthy subjects across a wide range of ages in an effort to design a set of tasks that can be administered quickly to obtain prototyping data for fMRI studies. The functional portion of the battery can be administered in approximately 20–25 min, and with additional modifications, the battery might be even shorter. All of the tasks were successful in activating at

Acknowledgment

This study was supported by SBIR grant R44 MH058504-03 from the NIMH.

References (46)

H.C. Breiter et al.
Response and habituation of the human amygdala during visual processing of facial expression
Neuron
(1996)
W.R. Crum et al.
Zen and the art of medical image registration: correspondence, homology, and quality
NeuroImage
(2003)
G. Fernandez et al.
Language mapping in less than 15 minutes: real-time functional MRI during routine clinical investigation
NeuroImage
(2001)
J.A. Fiez et al.
Linguistic processing
Int. Rev. Neurobiol.
(1997)
H. Fischer et al.
Age-differential patterns of brain activation during perception of angry faces
Neurosci. Lett.
(2005)
E. Formisano et al.
Tracking the mind's image in the brain: I. Time-resolved fMRI during visuospatial mental imagery
Neuron
(2002)
C.R. Genovese et al.
Thresholding of statistical maps in functional neuroimaging using the false discovery rate
NeuroImage
(2002)
S.A. Huettel et al.
Dynamic and strategic aspects of executive processing
Brain Res.
(2004)
B. Mazoyer et al.
Cortical networks for working memory and executive functions sustain the conscious resting state in man
Brain Res. Bull.
(2001)
R.A. Muller et al.
Are nonlinguistic functions in “Broca's area” prerequisites for language acquisition? fMRI findings from an ontogenetic viewpoint
Brain Lang.
(2004)

D. Sabatinelli et al.

Parallel amygdala and inferotemporal activation reflect emotional intensity and fear relevance

NeuroImage

(2005)

H. Steinmetz et al.

Functional anatomy of language processing: neuroimaging and the problem of individual variability

Neuropsychologia

(1991)

X. Wei et al.

Functional MRI of auditory verbal working memory: long-term reproducibility analysis

NeuroImage

(2004)

J. Wrase et al.

Gender differences in the processing of standardized emotional visual stimuli in humans: a functional magnetic resonance imaging study

Neurosci. Lett.

(2003)

P.A. Bandettini et al.

Characterization of cerebral blood oxygenation and flow changes during prolonged brain activation

Hum. Brain Mapp.

(1997)

R.R. Benson et al.

Language dominance determined by whole brain functional MRI in patients with brain lesions

Neurology

(1999)

J.R. Binder et al.

Human brain language areas identified by functional magnetic resonance imaging

J. Neurosci.

(1997)

R.G. Bittar et al.

Presurgical motor and somatosensory cortex mapping with functional magnetic resonance imaging and positron emission tomography

J. Neurosurg.

(1999)

W. Boling et al.

Localization of hand motor activation in Broca's pli de passage moyen

J. Neurosurg.

(1999)

R. Cabeza et al.

Imaging cognition II: an empirical review of 275 PET and fMRI studies

J. Cogn. Neurosci.

(2000)

D.B. FitzGerald et al.

Location of language in the cortex: a comparison between functional MR imaging and electrocortical stimulation

Am. J. Neuroradiol.

(1997)

A. Haberg et al.

Preoperative blood oxygen level-dependent functional magnetic resonance imaging in patients with primary brain tumors: clinical application and outcome

Neurosurgery

(2004)

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A rapid fMRI task battery for mapping of visual, motor, cognitive, and emotional function

Abstract

Introduction

Section snippets

Subjects

Subject compliance, head movement, and task performance

Discussion

Acknowledgment

Neuron

NeuroImage

NeuroImage

Int. Rev. Neurobiol.

Neurosci. Lett.

Neuron

NeuroImage

Brain Res.

Brain Res. Bull.

Brain Lang.

NeuroImage

Neuropsychologia

NeuroImage

Neurosci. Lett.

Characterization of cerebral blood oxygenation and flow changes during prolonged brain activation

Hum. Brain Mapp.

Language dominance determined by whole brain functional MRI in patients with brain lesions

Neurology

Human brain language areas identified by functional magnetic resonance imaging

J. Neurosci.

Presurgical motor and somatosensory cortex mapping with functional magnetic resonance imaging and positron emission tomography

J. Neurosurg.

Localization of hand motor activation in Broca's pli de passage moyen

J. Neurosurg.

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J. Cogn. Neurosci.

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Am. J. Neuroradiol.

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Neurosurgery