5 Creativity and the Brain’s Default Mode Network Marcus E. Raichle The purpose of this chapter is to explore some new ways of thinking about how the brain instantiates creativity. The route taken begins with an appraisal of the brain’s intrinsic or ongoing activity which, as I will explain, is the dominant mode of brain activity. A productive discussion of creativity must take into account the role of intrinsic activity. An important feature of this approach is to highlight the critical role of a recently discovered brain network, the default mode network (DMN), which serves in the organization of intrinsic activity and among whose component operations (i.e., memory and the adjudication of risk-taking) are im- portant elements of creativity. I begin with some general background material on intrinsic activity. Intrinsic Brain Activity Intrinsic activity refers to activity in all regions of the brain that is always pre- sent regardless of one’s state. It is present in conditions as varied as quiet repose with daydreaming to the full range of human behaviors. Intrinsic activity is also prominent during sleep. Intrinsic activity is easily observed with electrical recordings of brain activity obtained, for example, with electroencephalography (EEG). For those not fa- miliar with EEG, it is performed with a large array of electrodes placed over the scalp. A noteworthy observation concerning this activity was made in 1929, by the German psychiatrist Hans Berger who performed the first EEGs on human subjects.1 Introducing his new technique, he rhetorically asked “Is it possible to demonstrate the influence of intellectual work upon the human electroenceph- alogram, insofar as it has been reported here? Of course, one should not at first entertain too high hopes with regard to this, because mental work, as I explained elsewhere, adds only a small increment to the cortical work which is going on continuously and not only in the waking state.”2 Marcus E. Raichle, Creativity and the Brain’s Default Mode Network. In: Secrets of Creativity: What Neuroscience, the Arts, and Our Minds Reveal. Edited by Suzanne Nalbantian and Paul M. Matthews, Oxford University Press (2019). © Oxford University Press. DOI: 10.1093/oso/9780190462321.003.0006 108 Creativity and the Brain Berger’s prescient insight is strongly supported by an examination of the cost of brain function. In the average adult human, the brain represents about 2% of the total body weight yet it accounts for 20% of all the energy consumed,3 which is ten times that predicted by its weight alone. The energy cost of the developing human brain, which peaks at approximately the end of the first decade of life, approaches 50% of the total body energy consumption,4 which calls attention to the role of metabolism in brain development and plasticity across the lifespan, a subject relevant to creativity and one to which I will return later in this chapter. To put the high cost of intrinsic activity in perspective, it is important to note that the additional energy consumption associated with task- induced changes in brain activity is remarkably small, often less than 5% of a baseline level of activity locally.5 From these data it is clear that the brain’s enormous energy consumption is largely devoted to its intrinsic activity and little affected by task performance, an observation first made more than fifty years ago by Louis Sokoloff, Seymour Kety, and their colleagues6 but rarely cited. What other operational features attest to the functional importance of intrinsic activity? The processing of sensory information immediately comes to mind. As I sit before my computer composing this chapter, occasionally gazing out the window or surveying my office with its many interesting objects, I have no doubt about the richness of the details in the scene before me. Alas, it is an illu- sion! William James was one of the first to call attention to this fact,7 remarking 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.” More recently, the late Vernon Mountcastle, one of the twentieth century’s preeminent neurophysiologists, summed up the situation nicely: “Each of us believes himself to live directly within the world that surrounds him, to sense its objects and events precisely, and to live in real and current time. I assert that these are perceptual illusions. Sensation is an abstraction, not a replication, of the real world.”8 What facts sup- port such counterintuitive assertions? Complementary information comes from a consideration of the amount of sensory information made available to the brain. For example, it may surprise some to learn that visual information is significantly compressed as it passes from the eye to the visual cortex.9 Thus, of the information available from the environ- ment, only about 1010 bits/ s (i.e., 10 billion bits/s) are deposited in the retina. Yet, only 104 bits/ s (i.e., 0.001% of that which was deposited on the retina) make it to primary visual cortex. These data make it clear that visual cortex receives a very compressed representation of the world, a subject of more than passing interest to those seeking an understanding of visual information processing.10 Creativity and the Brain’s Default Mode Network 109 Parenthetically, it should be noted that estimates of the bandwidth of con- scious awareness itself (i.e., what we “see”) are in the range of 100 bits/ s or less.11 As Arthur Schopenhauer noted some time ago, “Consciousness is the mere sur- face of our mind, of which, as of the earthly globe, we do not know the interior, but only the crust.”12 One might add that from within the reservoir of the uncon- scious comes the makings of the “aha” moments of creativity.13 Given this striking perspective, it is interesting to look at research on the visual cortex of experimental animals during a nonstimulated state. What emerges is the appearance of a highly organized preparatory state. In a series of papers on the cat visual cortex using a combination of electrode recording and voltage sensitive dyes from the Weizmann Institute beginning in 1995,14 it was shown that the magnitude of ongoing intrinsic activity was the same as evoked activity and that the two interacted strongly, with the intrinsic activity contributing significantly to the variability in evoked activity, thus confirming an observation made many years before by George Bishop and Karl Lashley.15 And, even in the absence of stimuli, cortical representations of visual attributes emerged from the ongoing spontaneous activity.16 Elegant replications and extensions of this work have been contributed by others.17 Conceptual work on how these “simulations” might actually function has been provided by Schroeder and colleagues.18 Thus, combining a variety of perspectives on intrinsic activity reveals common themes at the cellular level and the full-brain, human systems level. At a very local level, at least in sensory cortices, intrinsic activity is functionally organized into the cortical representations of anticipated sensory attributes. At the human full- brain level, intrinsic activity is organized into systems well known for their participation in the full range of overt behaviors19 and prone, as well, to antici- pate incoming sensory information in preparation for responding.20 All of this work echoes prescient views of earlier scholars of brain function such as Thomas Huxley, Henry Maudsley, and William James.21 One of the pivotal events in moving us forward along these lines was the dis- covery of a large- scale, functional network organized within and potentially dominant over the brain’s intrinsic activity. I am referring to the brain’s DMN, whose discovery was an event of pure serendipity. The Default Mode Network The brain’s DMN was probably the most unexpected discovery of early func- tional imaging of the human brain. Anatomically, the DMN consists of a group of rather widely separated areas of the cerebral cortex (Figure 5.1A and 5.1C). 110 Creativity and the Brain (D) (A) (B) (E) (C) Figure 5.1 The group of brain areas (A) that decrease their activity during performance of a wide variety of tasks are often referred together as the brain’s default mode network (DMN). The spontaneous functional magnetic resonance image (fMRI) blood oxygen level dependent (BOLD) signal activity in the resting state (arrows, A) shows a remarkable similarity between regions of the DMN (B). For example, asking the general question of what areas in the brain are correlated with the activity in the back of the DMN (light arrow in [A] , light curve in [B]) reveals the entire DMN network (C). Analyses of other brain systems reveal similar levels of functional organization (D). Additional analyses suggest how resting-state activity propagates within and among brain networks. The image (E) shows anticorrelated relationships between the DMN and other systems collectively referred to as the task positive networks (TPNs), mediated by connectivity between the retrosplenial cortex (RSC) and the frontal eye fields (FEF). A–D adapted from Marcus Raichle, “The Restless Brain, How Intrinsic Activity Organizes Brain Function,”PhilosTrans R Soc B 370 (2015): 1– 11. E adapted from Michael Fox, et al., “The Human Brain Is Organized into Dynamic, Anticorrelated Functional Networks,” PNAS 102 (2005): 9673– 9678. Yet, despite their anatomical separation, the components of the DMN behave as a unit. Many readers of this chapter, especially those not working in the field of cog- nitive neuroscience, will immediately wonder what functionality the DMN instantiates and what it has to do with creativity.