In The Cognitive-Emotional Brain, Pessoa (Reference Pessoa2013) confronts the reader with the richness of what human neurosciences have achieved in the past decades and what these achievements imply for our understanding of human behavior and its neural underpinnings. A central aim of his book is to show that the often-applied conceptual dichotomy between “emotional” and “cognitive” brain regions is an incorrect view of how the brain is organized. Pessoa brings forth an abundance of studies showing that the neural substrates of cognition, on the one hand, and emotion, on the other hand, are largely shared, and by no means mutually exclusive. According to Pessoa, the brain should be understood from a network perspective: The function of the brain depends on its intrinsic connections rather than on specified brain modules. As such, Pessoa's view concurs with previous critiques of a modular brain (Panksepp & Panksepp Reference Panksepp and Panksepp2000; Prinz Reference Prinz and Stainton2006b) and with the currently popular idea that, more so than brain regions alone, it is the neural connections between these regions that are of main interest (Seung Reference Seung2012; Sporns Reference Sporns2010). Although we appreciate the breath of research addressed by Pessoa to convince his audience (and he surely convinced us), we were surprised to find that the book lacks a neuroevolutionary approach in describing brain function. We think this is a missed opportunity because a neuroevolutionary perspective illustrates why the distinction between emotion and cognition lacks theoretic ground and, thus, explanatory value.

In the human lineage, the most striking neural development is the vast increase in size of the neocortex. Evolved from the frontal part of the forebrain, the neocortex overlays the brainstem and limbic system, which consists of a set of brain regions (e.g., the amygdala and hypothalamus) shared by all mammalian species (MacLean Reference MacLean1990). The development of the anterior and dorsal part of the prefrontal cortex enabled people to mentally represent abstract information and to inhibit prepotent action tendencies, which gave rise to cognitive capacities such as foresight, planning, and selection of different behavioral responses. Together with increased linguistic capacities, this cortical development opened the door to modern culture (Munakata et al. Reference Munakata, Herd, Chatham, Depue, Banich and O'Reilly2011; Wilson Reference Wilson1998). However, the vast majority of the human cerebral cortex remains involved in unconscious processing of information from the environment and the viscera, which, through constant communication with phylogenetically older regions of the brain, can change our behavior without conscious deliberation (Damasio Reference Damasio2010). The neocortical expansion thus facilitated highly complex capacities often termed “cognitive,” but these capacities are still firmly rooted in the largely unconscious emotional brain. As such, cognition can be seen as the tip of the emotional iceberg. By definition, evolution builds on what is already there and is incapable of fundamental design changes in complex organisms. Thus, from a neuroevolutionary perspective there is not only no cognition without emotion, but this insight also provides the theoretical grounding for a network organization, instead of modular organization, of the brain.

A neural substrate that intriguingly exemplifies this mechanism of cumulative adaptation is the amygdala. The amygdala has often been regarded as a single subcortical structure, but animal work and recent advances in neuroimaging techniques show this view to be incorrect. In fact, the amygdala consists of many nuclei that resemble either subcortical (central and medial amygdala nuclei, CMA) or cortical (lateral and basolateral amygdala nuclei, BLA) cytoarchitecture. Considering the amygdala's location and structure, we believe it is the perfect candidate to integrate what Pessoa describes as “cognition” and “emotion.” Although Pessoa elaborates on the amygdala's heterogeneity, he seems to struggle to incorporate this feature in his network perspective of the brain. We believe that a neuroevolutionary view on amygdala functions will remedy this issue.

In terms of motivated behavior, two major amygdala network models can be identified. The first is a parallel model in which the cortical (BLA) and subcortical (CMA) amygdala respectively drive instrumental and impulsive goal-directed behavior through their projections to striatal and prefrontal structures (Balleine & Killcross Reference Balleine and Killcross2006; Phillips et al. Reference Phillips, Ahn and Howland2003). Second is a serial model in which information flows from BLA to hypothalamus and brain stem via CMA regions, which drives reflexive vigilance and fight-or-flight behavior (Whalen & Phelps Reference Whalen and Phelps2009). Recent evidence also indicates that the BLA not only feeds the CMA's initiation of vigilance but also exerts opposite influence that can reduce innate fear (Macedo et al. Reference Macedo, Martinez and Brandao2006; Reference Macedo, Martinez, Albrechet-Souza, Molina and Brandao2007; Tye et al. Reference Tye, Prakash, Kim, Fenno, Grosenick, Zarabi, Thompson, Gradinaru, Ramakrishnan and Deisseroth2011). Functional and structural MRI studies confirm these distributed networks of amygdala subregions in humans (e.g., Bickart et al. Reference Bickart, Hollenbeck, Barrett and Dickerson2012). Recent studies also confirmed the models' behavioral consequences, demonstrating that humans with focal damage to the BLA show increased fear vigilance (Terburg et al. Reference Terburg, Morgan, Montoya, Hooge, Thornton, Hariri, Panksepp, Stein and van Honk2012b) and more impulsive socioeconomic choices (van Honk et al. Reference van Honk, Eisenegger, Terburg, Stein and Morgan2013). Hence, a view emerges where the “cortical” amygdala (BLA) drives instrumental behavior and the “subcortical” amygdala (CMA) drives impulsive behavior. Thus, when combining the neuroevolution of the amygdala with recent evidence on its function and connectivity, the amygdala can be considered a key component of Pessoa's network perspective as a neural switch between impulsivity and deliberation. In this view, behavior cannot be considered distinctly “cognitive” or “emotional,” but will always be a cognitive-emotional synergy given the evolutionary organization of the brain.

This view of the amygdala as a neural “switch” extends even further when considering the endocrine regulation of amygdala function and connectivity (Bos et al. Reference Bos, Panksepp, Bluthe and Honk2012). For example, the steroid hormone testosterone and the neuropeptide oxytocin have opposite effects on amygdala output. When people are under direct social threat, testosterone decreases amygdala-cortical connectivity patterns and upregulates amygdala-subcortical routes (van Honk et al. Reference van Honk, Terburg and Bos2011b; Terburg & van Honk Reference Terburg and van Honk2013), whereas oxytocin reduces amygdala output to the brainstem (Stoop Reference Stoop2012) and increases amygdala-cortical coupling (Riem et al. Reference Riem, Bakermans-Kranenburg, Pieper, Tops, Boksem, Vermeiren, van IJzendoorn and Rombouts2011). Moreover, both hormones have been involved in sexual and reproductive behavior in animal species living as long as 450 million years ago (Bryan et al. Reference Bryan, Scott and Li2008; Goodson & Bass Reference Goodson and Bass2001), and these functions have been conserved in humans. In line with the evolutionary development of the amygdala and the neuroendocrine system, the behavioral impact of these hormones has extended to more diverse human behavioral repertoires. Following evidence that testosterone promotes social, but not predatory, aggression (Archer Reference Archer2006), recent testosterone studies have focused on human dominance behavior. Being the leader of the pack provides evolutionary advantages by increasing chances of survival, and testosterone indeed not only promotes emotional-reflexive (Terburg et al. Reference Terburg, Aarts and van Honk2012a) but also cognitive-strategic (Eisenegger et al. Reference Eisenegger, Naef, Snozzi, Heinrichs and Fehr2010; van Honk et al. Reference van Honk, Montoya, Bos, van Vugt and Terburg2012) dominance behavior. In addition, testosterone in humans has recently been shown to affect even more complex social behaviors; for example, it reduces interpersonal trust (Bos et al. Reference Bos, Terburg and van Honk2010), reduces cognitive empathy (van Honk et al. Reference van Honk, Schutter, Bos, Kruijt, Lentjes and Baron-Cohen2011a), and promotes utilitarian decision making (Montoya et al. Reference Montoya, Terburg, Bos, Will, Buskens, Raub and van Honk2013). As predicted based on its opposite effects on amygdala function, oxytocin has opposite effects to those of testosterone; it increases interpersonal trust (Kosfeld et al. Reference Kosfeld, Heinrichs, Zak, Fischbacher and Fehr2005) and increases cognitive empathy (Domes et al. Reference Domes, Heinrichs, Michel, Berger and Herpertz2007). Thus, the neuroendocrine messengers that have evolved to serve basic emotional processes throughout the animal kingdom have come to serve complex, allegedly “cognitive,” functions in humans. They do so by acting on ancient brain “hubs” and “switches,” thereby leaving no brain areas unaffected.

In agreement with Pessoa, this literature highlights the difficulties, if not impossibility, of defending a view in which parts of the brain are discussed in terms of their unique functions. We suggest that a neuroevolutionary approach in discussing brain function provides for a theoretic reason for rejecting the “emotion-cognition” dichotomy and also provides a theoretical grounding for a network organization, instead of a modular organization, of the brain. In addition, Pessoa (Reference Pessoa2013) notes that “more than making the case against dissociating [emotion and cognition], one of my goals in this book is to move beyond the debate and to illustrate the many ways in which emotion and cognition interact and in fact are integrated” (p. 3). We fully agree with Pessoa that the emotion-cognition dichotomy is one in need of revision, but we wonder if Pessoa's focus on cognition-emotion interactions might inadvertently keep the false dichotomy alive. We believe that a neuroevolutionary perspective, which sees cognition as the tip of the emotional iceberg, provides a solution to definitely move beyond this debate and allows us to focus on explaining how the brain brings forth behavior, irrespective of the terminology that is used to describe this behavior.