Decision making: the neuroethological turn

Abstract

Neuroeconomics applies models from economics and psychology to inform neurobiological studies of choice. This approach has revealed neural signatures of concepts like value, risk, and ambiguity, which are known to influence decision making. Such observations have led theorists to hypothesize a single, unified decision process that mediates choice behavior via a common neural currency for outcomes like food, money, or social praise. In parallel, recent neuroethological studies of decision making have focused on natural behaviors like foraging, mate choice, and social interactions. These decisions strongly impact evolutionary fitness and thus are likely to have played a key role in shaping the neural circuits that mediate decision making. This approach has revealed a suite of computational motifs that appear to be shared across a wide variety of organisms. We argue that the existence of deep homologies in the neural circuits mediating choice may have profound implications for understanding human decision making in health and disease.

Figure 1

Comparison of foraging across species. A. Alternation between dwelling and roaming behaviors by C. elegans, under the control of serotonin and the neuropeptide pigment dispersing factor (PDF) (adapted from(Flavell et al., 2013)) B. Egg laying behavior by drosophila varies between nutrient rich and nutrient poor areas in a manner displaying exquisite sensitivity to the costs and benefits implicit moving from one patch of agar to the next (Yang et al., 2008). C,D, and E show neural activation in rodents, non-human primates, and humans, respectively, in versions of the patch-leaving paradigm (Hayden et al., 2011; Kolling et al., 2012; Kvitsiani et al., 2013). In each case, heightened activity in the dorsal anterior cingulate cortex signals an imminent switch away from the current default option. This suggests not only a remarkable degree of behavioral consistency across taxa, with similar decision algorithms across species, but a neural consistency within mammals.

Figure 2

Putative exaptation of foraging-related behaviors to serve social function in primates. A. Parallel channels for processing social and non-social reinforcers in the primate striatum. Neurons responsive to social rewards are located more medially, whereas neurons responsive to fluid rewards are more lateral. Normalized firing profile of two example neurons in the striatum that differentiate between a single type of reward. Left panels, trials separated by image category; right panels, trials separated by fluid amount. Decision task consisted of a central fixation, a saccade towards a decision target, delivery of juice reward, and an optional image display. Time histograms are aligned to proximate events. Insets illustrate location of each recorded neuron. Reproduced from (Klein and Platt, 2013) B. Facial muscle activity and BOLD activity evoked by aversive gustatory or social outcomes. Top left, activity of the levator labii muscle in the face produces the wrinkled nose characteristic of disgusted facial expression. Top middle, BOLD activity elicited after viewing a disgusting ingestive stimulus (video of an individual gagging and eating raw condensed canned soup) overlaps with BOLD activity correlated with tachygastria, fluctuations of gut activity. This demonstrates the relationship between the experienced emotion of disgust and the state of the digestive system (Harrison et al., 2010). Top right right, BOLD activity associated with receiving unfair offers in the Ultimatum game, a proxy for social/moral disgust (Sanfey et al., 2003). Bottom, similar patterns of facial activity are produced when tasting a bitter substance (bottom left), viewing a disgusting picture (bottom middle), or receiving an unfair offer in the Ultimatum game (bottom right). Modified with permission from (Chapman et al., 2009). These findings suggest a relationship between food avoidance and social avoidance behaviors.

Figure B1

The terms “vmPFC” and “OFC” are used inconsistently within and across subfields of neuroscience. A. Anatomically delineated regions of OFC have high correspondence between humans (left) and macaques (right). Reproduced with permission from (Mackey and Petrides, 2010). Based on non-human primate neuroanatomy, OFC proper corresponds to all colored brain areas, except 10, 24, 25, and 32. B. Nearly identical brain coordinates are described both as vmPFC, left (data from (Levy and Glimcher, 2012), coordinates illustrated using Neurosynth) and OFC (from (Cox et al., 2005)). C. vmPFC is a descriptive term, and is used in the neuroeconomics literature to refer to regions in the OFC, ACC, and the nearby medial wall (reproduced from (Hare et al., 2009), illustrating data from previous studies [dark blue (Kable and Glimcher, 2007), light blue (Rolls et al., 2008), red (Plassmann et al., 2007), and green (Hare et al., 2008)].