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Web Topic 8.7
Brains and Decision Making

Overview

One of the most exciting developments in the last decade is the increasing ability to monitor the neurobiology of decision makers. In animals, this has traditionally involved inserting electrodes into selected brain areas and monitoring relative activity as the animal makes a decision. Recent technical advances such as two-photon imaging and optogenetics have pushed the envelope even further by identifying events at the individual neuron and sub-neuron levels (Homma et al. 2009; Knopfel et al. 2010). Popular animal systems include roundworms, sea slugs, leeches, honeybees, zebrafish, zebra finches, mice, rats, and monkeys. In people, non-invasive functional magnetic resonance imaging (fMRI) uses the increased metabolic activity of working neurons to track the steps as a person makes different kinds of decisions. These technologies have encouraged neurobiologists to determine whether animals or people really have the necessary machinery for Bayesian updating and optimal decision making, or instead are just relying on some very clever heuristics. They also have looked for possible causes for the biases seen in animal and human decision making. Suitable areas of the brain for these functions have now been located in animals and humans, and this has encouraged a melding of economics and neurobiology into a field called neuroeconomics (Glimcher and Rustichini 2004).

Basic structure of the human brain

The human brain is divided into a series of lobes and internal regions (Figure 1):

Figure 1: (A) The four lobes of the human cerebral cortex and some of their functions. Decision making involves the most anterior (near the face) parts of the frontal lobes, parts of the parietal lobes, and deep inside, parts of the temporal lobes. (B) Top view of human cerebral cortex. Note that the brain is largely divided into left and right hemispheres. Decisions based on more confident probability and payoff estimates tend to activate relevant areas in the left hemisphere; less certain decisions may activate the corresponding regions but in the right hemisphere.

The large and prominently fissured mass on the top is called the cerebrum or cortex. It is divided at most points into right and left hemispheres. Each hemisphere hosts four regions called lobes. While each lobe is in fact multifunctional, one can roughly assign reasoning and voluntary movements to the frontal lobe, audition and some higher level visual processing to the temporal lobe, touch and skin sensations to the parietal lobe, and vision to the occipital lobe. Deep inside the folds in each hemisphere where the temporal and frontal lobes meet are the insula; these deal with visceral functions and taste. Below the cortex is a complex of regions known as the subcortex. This includes the striatum (also known as the basal ganglia), which consists of two parallel structures that begin in the frontal lobe and arc backwards into each temporal lobe, down, and then forwards again. (Figure 2).

 

Figure 2: The basal ganglia (collectively called the striatum) are located in the center of the brain just below the outer cortex. The major components are the caudate nucleus, the putamen, and the globus pallidus. The ventral striatum (an important area that stores utility values for rewards of actions) consists of ventral and medial parts of the caudate nucleus and the putamen.

This area starts, regulates, and stops voluntary motor actions. Interdigitated with the striatum is another set of subcortical structures called the limbic system (Figure 3):

Figure 3: The limbic system (dark orange in picture) is located in the same subcortical region as the basal ganglia and the two actually wrap around each other. The major components are the cingulate gyrus, an arcing region in each hemisphere at the top of the subcortex, the amygdala and the hippocampus in the lower region of each temporal lobe, and the hypothalamus in the center. Many parts of the prefrontal cortex and the ventral striatum interact extensively with the limbic system during decision making. The ventral striatum is thought to store weighted reward payoff information, and the amygdala to store weighted costs. The hippocampus oversees the storage of memories, including templates of signals and cues that are associated with payoffs and probabilities. The hypothalamus generates “somatic marker” physiological responses to stimuli. The anterior region of the cingulate seems to monitor all decision making, at times helping focus on rational decisions, and at others, alerting the rest of the brain that actual payoffs are different from expected values. The prefrontal lobes play major roles in comparing probabilities, payoffs, and expected values.

These include the cingulate cortex which is a large band above the striatum, and the amygdala and hippocampus zones in the lower parts of each temporal lobe. The limbic system controls emotion (cingulate and amygdala) and regulates what gets stored as memories in the brain (hippocampus). The cerebrum connects to the spinal cord successively through the diencephalon, the midbrain, and the brainstem, all of which handle switching and routing functions for nerve traffic coming into and out of the brain. The lower part of the diencephalon, the hypothalamus, regulates a number of autonomic functions such as body temperature, hunger, thirst, reproduction, and circadian rhythms. The brainstem hosts two systems that modulate activity throughout the brain using specific transmitter substances. One, the dopamine system, plays an important role in assigning reward values to recent stimuli. The second, the norepinephrine system, modulates mental arousal and vigilance. The cerebellum, which controls posture, coordination, and balance, is nestled between the cortex and the midbrain at the rear of the brain.

Rational decision making in human brains

Economists and psychologists had speculated that the brain might have two separate decision-making systems: one, that was fast and heuristic, and a second, that was slower but more rational (Kahneman and Tversky 2000; Camerer et al. 2005). The reality has turned out to be a bit more complicated (McClure et al. 2004; Glimcher et al. 2005; Sugrue et al. 2005; Trepel et al. 2005; Sanfey et al. 2006). Some parts of the brain, such as the prefrontal areas of the frontal lobes, seem to be active during any decision process. There are three (at least) sub-regions within the prefrontal cortex that are activated during decision making (Figure 4). The ventromedial zone is independently sensitive to changes in outcome probabilities and payoffs, but also contributes to their combination as expected values (Knutson et al. 2005; Daw et al. 2006; Sanfey et al. 2006). The adjacent orbitofrontal zone seems involved with contrasts between alternative possible payoffs, but may focus more on losses (and aversive actions) than on gains (and appetitive actions) (O’Doherty et al. 2003; Ursu and Carter 2005; Daw et al. 2006). The dorsolateral zone also appears to track current estimates of expected values and is tightly linked to a final decision zone in the posterior part of the parietal lobe (Kim and Shadlen 1999; Trepel et al. 2005; Sanfey et al. 2006).

Figure 4: Prefrontal lobe regions of human brain activated during decision making. See text for specific roles in this process.

Activity in this latter area remains sensitive to changes in probabilities and payoffs of alternative consequences suggesting that final commitments to action do not take place earlier in the prefrontal regions (Glimcher 2003; Glimcher et al. 2005; Sugrue et al. 2005). Once this parietal region is activated, the next step is performance of an action. Many of these steps may be lateralized: when probabilities and payoffs are relatively certain, the relevant parts of the left hemisphere handle the decision making; when alternatives are equally likely or probabilities are uncertain, the relevant regions in the right hemisphere dominate the decision process (Kim et al. 2004; Knutson et al. 2005). These and similar studies have verified the existence of explicit brain regions that can track probabilities, payoffs, and expected values for multiple alternatives and compare them for rational decision making.

Biased decisions in human brains

What happens when decisions are less than rational? Instead of invocation of a second and separate decision system, recent research suggests that biased decisions are generated when other brain centers such as the limbic system and striatum modulate the rational process (McClure et al. 2004; Yarkoni et al. 2005; Sanfey et al. 2006; Tom et al. 2006). The ventral striatum appears to be a general repository of positive (gain) payoff information (O’Doherty et al. 2004; Knutson et al. 2005; Daw et al. 2006). The amygdala has been proposed as a general repository of negative (loss) payoff information (Dalgleish 2004). Neither site appears to store absolute payoff values but instead converts estimates into “utilities” as a function of the current physiological state of the animal, levels of risk, the degree to which contexts limit choice, and historical associations with similar situations. The striatum and amygdala have tight links to the ventromedial and orbitofrontal prefrontal zones respectively where their weighted utility estimates are then played against the more direct estimates of rational decision making. The degree to which the decision is rational appears to depend on the strength of striatal and amygdala inputs relative to the ongoing rational process (McClure et al. 2004; De Martino et al. 2006). Note that the processing of losses and gains in separate brain regions could explain the observed higher biases for losses than for gains if the influence of the amygdala were generally greater than that of the ventral striatum.

Recent fMRI studies indicate that the amygdala is a primary source of risk sensitivity and framing biases (De Martino et al. 2006). A second source of decision bias is the presence of somatic markers (Bechara and Damasio 2005). Somatic markers are combinations of autonomic responses such as accelerated heart rate, perspiration, heat and cold flashes, or general muscle tension that are triggered (usually by the hypothalamus) when certain kinds of signals or cues are perceived by the decision maker. Some somatic markers are instinctive, whereas others are acquired from prior experience. They provide one possible mechanism for invoking the past in a linear operator process. When activated, a somatic marker acts as an additional cue that the ventromedial prefrontal cortex needs to consider during its melding of direct estimates and input from the striatum and amygdala.

Much of the remaining decision machinery in the mammalian brain seems to be devoted to updating and error correction following a decision. Once an action is complete, the prefrontal cortex, amygdala, and striatum all receive input that allows them to compare the actual versus previously anticipated payoffs. When there is a large difference between these values, the anterior cingulate, which is an active observer of all decision making, and the orbitofrontal cortex alert the brain to this situation; a particularly strong difference between expected and observed payoffs may also activate the insula (O’Doherty et al. 2003; Dalgleish 2004). If the rewards of the action exceed expectations, the dopamine system in the brainstem increases its activity, and if rewards are less than expected, then the dopamine system reduces its activity (Pessiglione et al. 2006). Where observed and expected rewards are similar, the dopamine system activity remains unchanged. Because the dopamine system projects throughout the brain, this provides a global broadcast of the effectiveness of the latest decision (Schultz 1998). The amygdala, striatum, and the dorsolateral cortex then play key roles in updating stored payoffs based on this recent experience. In this context, the amygdala is thought to rescale both gain and loss payoffs into weighted utilities and then feed these biases to the orbitofrontal cortex (Dalgleish 2004; De Martino et al. 2006; Paton et al. 2006). The dorsal striatum is also involved in updating once actual payoffs can be evaluated, and may play a role in establishing heuristic short cuts for future encounters (O’Doherty et al. 2004). Finally, the hippocampus and other nearby regions of the temporal lobe oversee the updating or addition of memory templates for any recent cues or signals that facilitated the decision (Greene et al. 2006; Moscovitch et al. 2006; Svoboda et al. 2006).

Other vertebrate brains and decision making

The basic brain structures and functions described above appear to be shared among rats, monkeys, and humans. What about other vertebrates? Until recently, the regions of birds’ brains followed a completely different nomenclature. Careful comparisons have now revealed that there are very strong parallels in avian and mammalian brains, and most of the structures identified above for mammals are now believed to have counterparts in the brains of birds (Jarvis et al. 2005). Since birds and mammals show similar evidence of rational decision making and similar biases when irrational, it seems likely that neurobiologists will eventually demonstrate similar processes in both taxa. Although amphibians have a much smaller cerebrum than birds or mammals, they also share many of the subcortical structures described earlier including basal ganglia, amygdala, striatum, hippocampus, and hypothalamus (Striedter 1997; Endepols et al. 2005; Medina et al. 2005). Several of these structures even appear to be present with similar functions in fish (Broglio et al. 2005; Portavella and Vargas 2005). This suggests that the basic processes of decision making evolved early in the vertebrate line and have only been elaborated by subsequent evolution (see also the multiple chapters relating brain regions to specific ecological and behavioral tasks in Dukas and Radcliffe 2009).

Invertebrate brains and decision making

Invertebrates have quite different brain structures from vertebrates. However, research on slugs and leeches suggests that successive stimuli lead to cumulative updating, and that decisions depend on mutual levels of activity in multiple nerve cells as opposed to simple association and switching circuits (Esch and Kristan 2002; Esch et al. 2002; Jing and Gillette 2003; Briggman et al. 2005). The brains of most insects consist of sensory processing ganglia that provide input to mushroom bodies where associative learning and decision making take place (Fahrbach 2006; Menzel et al. 2006). While there has yet been little neurobiological work on decision making in insects, genetic and biochemical studies suggest that decisions again involve multiple but interacting regions within the mushroom bodies (Heberlein et al. 2004; Abramson et al. 2005).

Figure 5: The brain of a honeybee. The large masses (ME and LO) on each side do most of the processing of visual stimuli. Olfactory stimuli are processed in the paired lobes on the bottom side of the brain (AL). Decision making and memory appear to be the main functions of the large mushroom bodies (MC and LC) positioned at the top and between the various sensory lobes. (After Menzel 1983.)

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