Frontal Lobe Functioning in Man: The Riddle Revisited
Archives of Clinical Neuropsychology
Frontal Lobe Functioning in Man: The Riddle Revisited
Sergio Della Sala 0 1
Colin Gray 0 1
Hans Spinnler 0 1
0 University of Aberdeen , UK
1 S. Paolo Hospital, University of Milan , Italy
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Forty-eight patients, each with a single frontal lobe lesion, were tested with a battery of 10 of the
most widely used neuropsychological tests, comprising five traditional “frontal” tests and five
others, for which that claim is not generally made. All correlations among the tests in the group
were positive and significant. Moreover, the average correlation between each frontal test and
the other tests in the frontal group was found to be higher than the average correlation of the
same frontal test with the tests in the other group. A factor analysis of the scores on the five
frontal tests yielded a single factor accounting for 53% of the variance. A factor analysis on the
entire battery of tests (frontal plus nonfrontal) also yielded a strong general factor; although this
accounted for a smaller portion (43%) of the shared variance, and one test (Verbal Span) failed
to show a substantial loading on the factor. Neither the results of the present study nor the
findings of other researchers argue for the abandonment of the concept of “executive” functioning,
mediated by the functioning of the frontal lobes, in favor of a variant of fractionation. © 1998
National Academy of Neuropsychology. Published by Elsevier Science Ltd
After a century and a quarter of research, the function of the frontal regions of the brain
continues to be the subject of speculation, and of controversy. In the 1960s, Teuber,
summing up the state of knowledge at the time, wrote of “the riddle of frontal lobe
function in man”
(Teuber, 1964, p. 410)
. Today, some 30 years later
(and over 125 years after
the publication of the puzzling case history of Phineas Gage [Harlow, 1868; see
Damasio, Grabowski, Frank, Galaburda, & Damasio 1994])
, the riddle has yet to be solved
(review in Darling, Della Sala, Gray & Trivelli, in press).
The so-called “riddle of the frontal lobes” is, in fact, not one puzzle but a whole set of
related questions, some theoretical, others methodological. The former are concerned
with the nature of frontal lobe functioning, the latter with its measurement. In recent
years, there has been much consideration of whether there is essentially one kind of
prefrontal lobe activity that is brought into play whenever any of a wide category of tasks is
undertaken or, on the contrary, there are many different frontal functions, each of which
is required only for a relatively narrow range of tasks. It is this issue with which the
present paper is primarily concerned.
The case histories of those who have sustained frontal damage are certainly
perplexing. On the one hand, as with Harlow’s famous patient Phineas Gage
(Harlow, 1868)
,
and with many similar cases described subsequently
(e.g., Eslinger & Damasio, 1985)
,
the cognitive effects of frontal damage are often by no means immediately apparent.
The patient may appear to function much as before, with little or no obvious mental
deterioration; in fact, some frontal patients show high levels of psychometric intelligence
(Brazzelli, Colombo, Della Sala, & Spinnler, 1994; Shallice & Burgess, 1991)
. On the
other hand, while a variety of other sequelae have been reported in frontal patients,
each occurs in some patients but not in others, making it difficult to discern an
underlying pattern. For example, some patients show personality change
(Ackerly & Benton,
1948; Brickner, 1936; Penfield & Evans, 1935)
, but others may not (Hebb & Penfield,
1940). There are, however, certain recurring themes. Although one patient may show an
uncharacteristic apathy, another may present a contrasting picture of puerile practical
joking and disinhibited social behaviour, and a third may display both of these
contrasting patterns at different times
(Blumer & Benson, 1975)
, the occurrence of at least one
of these presentations is so common in patients with damage to the frontal cortex that
they are often referred to by clinicians as “frontal lobishness”
(Benson, 1994)
.
In contrast with the frequency of the global patterns of frontal lobishness, the search
for specific cognitive deficits peculiar to frontal lobe patients has generally been
unrewarding. Following the discovery, in the 19th century, of Broca’s area, and of evidence
to suggest that the frontal lobes are involved in the coordination of the motor
movements involved in voluntary actions
(Bianchi, 1895; Jastrowitz, 1888)
, little else of
interest was reported for several decades until, in the late 60s and 70s, Milner and her
associates published some work suggesting that certain regions in the prefrontal lobes
controlled specific functions (e.g., Jones-Gotman & Milner, 1977). Patients with frontal
excisions involving the dorsolateral areas made more errors on the Wisconsin Card
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