Intrinsic Activity and
the Brain's Dark Energy
In the adult human the brain represents about 2 percent
of the body weight yet accounts for about 20 percent of
its energy consumption, ten times that predicted by its
weight alone. A critical question is: What fraction of
this large energy budget is directly related to its functions?
The answer is, the majority. Depending on the approach
used, it is estimated that 60 percent-80 percent of the
energy budget of the brain is devoted to its functional
activity. This occurs in the form of ongoing events associated
with the input and output of neurons, large and small,
and the activity in astrocytes in direct support of these
processes.
How does this overall cost of brain functions compare
to the cost of changes in brain functions elicited by
responses to controlled stimuli? Brain-imaging data provide
useful, quantitative measures of the cost of changes in
brain activity. But it should be noted that inferences
derived from the analysis apply broadly across all levels
of neuroscience when changes in activity to controlled
stimuli are studied.
Brain-imaging signals, whether produced from PET or fMRI
arise from a change in local blood flow that accompanies
changes in the local cellular activity of the brain. While
PET measures changes in blood flow directly, fMRI senses
the changes in local blood oxygen content that arise because
blood flow alters more than local oxygen consumption.
Thus, the fMRI signal is known as the blood oxygen-level
dependent, or BOLD, signal.
The regional increases in absolute blood flow associated
with imaging signals as measured with PET are rarely more
than 5 percent-l0 percent of the resting blood flow of
the brain. However, the actual increase in energy consumption
associated with these circulatory changes may be as little
as 0.5 percent-1.0 percent. These are modest modulations
in ongoing circulatory activity that rarely affect the
overall rate of brain blood flow during even the most
amusing perceptual and vigorous motor activity. From this
analysis it becomes clear, then, that the brain continuously
expends a considerable amount of energy for functions
even in the absence of a particular task (i.e., when a
subject is awake and at rest).
From this cost-based analysis of the brain's functional
activity it seems reasonable to conclude that intrinsic
activity may be as significant, if not more so, than evoked
activity in terms of overall brain function. Taking this
position converts one's view of the brain from a system
primarily responding to external inputs (the traditional
view motivating most neuroscience research) to one operating
on its own, intrinsically, with sensory information interacting
with rather than determining the operation of the system.
Historically, this view has received support from many
quarters. It was William James who, in 1890, presciently
suggested to the readers of his Principles of Psychology
that "enough has now been said to prove the general law
of perception, which is this, that whilst part of what
we perceive comes through our senses from the object before
us, another part (and it may be the larger part) always
comes (in Lazarus's phrase) out of our own head." In his
book of the Vortex: From Neurons to Self, Rodolfo Llinas
more recently summarized the evidence for this point of
view, beginning with the work of early twentieth-century
physiologists through his own contemporary contributions.
He concluded that the significance of incoming sensory
information depends on the pre-existing disposition of
the brain, [which] is a far deeper issue than one gathers
at first glance
