Relative Shift in Activity from Medial to Lateral Frontal
Cortex During Internally Versus Externally Guided
Word Generation
Bruce Crosson, Joseph R. Sadek, Leeza Maron, Didem Go ¨kc¸ay,
Cecile M. Mohr, Edward J. Auerbach, Alan J. Freeman,
Christiana M. Leonard, and Richard W. Briggs
Abstract
& Goldberg (1985) hypothesized that as language output
changes from internally to externally guided production,
activity shifts from supplementary motor area (SMA) to lateral
premotor areas, including Broca’s area. To test this hypothesis,
15 right-handed native English speakers performed three word
generation tasks varying in the amount of internal guidance
and a repetition task during functional magnetic resonance
imaging (fMRI). Volumes of significant activity for each task
versus a resting state were derived using voxel-by-voxel
repeated-measures t tests (p < .001) across subjects. Changes
in the size of activity volumes for left medial frontal regions
(SMA and pre-SMA/BA 32) versus left lateral frontal regions
(Broca’s area, inferior frontal sulcus) were assessed as internal
guidance of word generation decreased and external guidance
increased. Comparing SMA to Broca’s area, Goldberg’s
hypothesis was not verified. However, pre-SMA/BA 32 activity
volumes decreased significantly and inferior frontal sulcus
activity volumes increased significantly as word generation
tasks moved from internally to externally guided. &
How does the human brain initiate the expression of
thought in language? A comprehensive understanding
of the brain’s language systems necessitates an answer
to this question. An appreciation of language initiation
mechanisms could facilitate treatment development for
language initiation deficits in aphasia. For some time,
cognitive neuroscientists have known that the medial
frontal cortex plays a role in language initiation. How-
ever, the nature of this involvement has yet to be
determined.
Medial frontal lesions cause akinetic mutism, in
which speech is initiated only with significant external
prompting (Barris & Schuman, 1953; Nielson & Jacobs,
1951). Regarding the absence of spontaneous lan-
guage, Luria’s (1966) report of a medial frontal lesion
case indicated that thoughts were not present to
express. This phenomenon suggests that the medial
frontal cortex plays a role in initiating the cognitive
aspects of spontaneous language. After evaluating em-
pirical evidence on this subject, Picard and Strick
(1996), Passingham (1993), and Goldberg (1985) con-
cluded that the degree of involvement of medial
frontal structures, and which medial structures partici-
pate, depends upon the nature of the language that is
initiated.
Goldberg (1985) suggested that involvement of med-
ial frontal cortex depends upon whether language is
triggered by internal or external contingencies. He fo-
cused on the divergent roles of the supplementary
motor area (SMA) and lateral premotor cortex. Goldberg
speculated that Broca’s area was prominent in the lateral
premotor cortex of humans (p. 578), especially when
considering language functions. Traditionally, Broca’s
area has been designated as the posterior portion of
the inferior frontal gyrus, i.e., pars opercularis (Brod-
mann’s area [BA] 44) and pars triangularis (BA 45).
Although recent literature indicates important functional
divisions within medial BA 6 that might have influenced
his conclusions (see below), SMA was considered to
consist of the entire medial BA 6 at the time Goldberg
wrote his review. He surmised that SMA was primarily
involved in internally generated language and actions,
whereas lateral premotor cortex was involved in lan-
guage or actions that are externally referenced.
Passingham’s (1993) subsequent review on medial
versus lateral premotor cortex arrived at a similar con-
clusion. In reference to selection of movement, Passing-
ham believed that lateral premotor cortex made greater
contributions when movements were driven by external
cues, and medial premotor cortex played a greater role
when no external cues were available (i.e., when move-
ment was driven from internal models). However, Pas-
singham (1993) also concluded that neither internally University of Florida
© 2001 Massachusetts Institute of Technology Journal of Cognitive Neuroscience 13:2, pp. 272–283