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The Adaptive Nature of the Human Neurocognitive Architecture: an Alternative Model Proc. Natl. Acad. Sci. USA Vol. 95, pp. 11290–11294, September 1998 Evolution The adaptive nature of the human neurocognitive architecture: An alternative model PEGGY LA CERRA* AND ROGER BINGHAM†‡ *1333 Garden Street, Santa Barbara, CA 93101; and †Division of Biology, California Institute of Technology, Pasadena, CA 91125 Communicated by George C. Williams, State University of New York at Stony Brook, Stony Brook, NY, July 9, 1998 (received for review March 18, 1998) ABSTRACT The model of the human neurocognitive ar- providing support for the hypothesized domain-specific mech- chitecture proposed by evolutionary psychologists is based on anisms under investigation, the absence of a definitive analysis the presumption that the demands of hunter-gatherer life (i.e., a method that parses out the possible contributions of the generated a vast array of cognitive adaptations. Here we other postulated mechanisms, specific and general), makes present an alternative model. We argue that the problems such conclusions, at best, speculative. inherent in the biological markets of ancestral hominids and Within the theoretical framework of evolutionary psychol- their mammalian predecessors would have required an adap- ogy, the critical problem of the adaptive selection of behavior tively flexible, on-line information-processing system, and rests heavily on the integrative circuitry that is presumed to would have driven the evolution of a functionally plastic engage the appropriate domain-specific mechanism. Yet, like neural substrate, the neocortex, rather than a confederation the postulated domain-general mechanisms, this circuitry re- of evolutionarily prespecified social cognitive adaptations. In mains theoretically unconsidered and empirically unexplored alignment with recent neuroscientific evidence, we suggest within the paradigm. that human cognitive processes result from the activation of An obvious source of information that might illuminate constructed cortical representational networks, which reflect these hypothetical mechanisms is the extensive neuroscientific probabilistic relationships between sensory inputs, behavioral literature on the biological basis of adaptive behavior in responses, and adaptive outcomes. The developmental con- mammals. But evolutionary psychologists have suggested that struction and experiential modification of these networks are analysis at the implementation level (i.e., investigation of the mediated by subcortical circuitries that are responsive to the neural correlates of behavior) is not mandatory for the study life history regulatory system. As a consequence, these net- of cognitive adaptations (7, 8). In our view, this failure to works are intrinsically adaptively constrained. The theoretical reconcile theoretical claims with neurobiological data has and research implications of this alternative evolutionary veiled from evolutionary analyses the functional organization model are discussed. of the information-processing circuitries that comprise the human neurocognitive architecture. Indeed, the alternative, neurobiologically based model we present here compels a An extensive literature underscores the enormous functional y y plasticity of the neocortex (1–3), a distinguishing characteristic reconceptualization of the domain-specific domain-general of mammals (1, 4). This evidence supports the position that integrative circuitry constructs as they are currently employed cortical representational features are systematically con- by evolutionary behavioral scientists. structed by the dynamic interaction between environmentally Reconceptualizing the Nature of Social Adaptive Problems derived neural activity and intrinsic neural growth mechanisms and Solutions (3). The information-processing capacities of the neocortex are largely constructed by the problem domains confronting the Evolutionary psychologists have appropriately acknowledged individual throughout development, and remain modifiable the importance of adaptive social behavior to the inclusive throughout the life history. This neurobiological constructivist fitness of hominids. Recognizing the complexity of the ances- account of the human neurocognitive architecture contrasts tral social environment, they propose that humans have in- sharply with the account of evolutionary psychologists, who herited a vast array of cognitive adaptations that facilitated conceive of the mind as a confederation of information- social negotiations. Examples include postulated domain- processing adaptations, each of which evolved in response to specific adaptations to detect ‘‘cheaters’’ (9); to ‘‘have an a problem posed by Pleistocene selection pressures (5). appetite to be recognized and valued for [one’s] individuality Numerous methodological problems and theoretical flaws or exceptional attributes’’; and to ‘‘be motivated to cultivate call the validity of the evolutionary psychological paradigm specialized skills, attributes, and habitual activities that in- into question (6). Its proponents claim that three categories of crease [one’s] relative irreplaceability,’’ etc. (10). In contrast, evolved mechanisms support human intelligence—domain- we suggest that a functionally plastic neocortex was the evo- specific mechanisms, domain-general mechanisms, and an lutionary solution to the adaptive navigation of ancestral social integrative circuitry—but their research programs have fo- environments. [In fact, other researchers have proposed that cused exclusively on generating evidence for postulated do- the evolutionary appearance of the neocortex in mammals was main-specific mechanisms. The standard protocol involves the consequence of navigating fluctuating environments (11– assessing subjects’ relative performance on tasks that vary in 14)]. the degree to which they correspond to an inferred ancestral In game theoretic models of biological market dynamics, adaptive problem. Although results that align with predicted various classes of traders exchange commodities to their patterns of reasoning performance have been interpreted as mutual benefit (15–17). Biological market models are charac- terized by competition within trader classes by contest or The publication costs of this article were defrayed in part by page charge payment. This article must therefore be hereby marked ‘‘advertisement’’ in Abbreviation: VUMmx1, ventral unpaired median cell of maxillary accordance with 18 U.S.C. §1734 solely to indicate this fact. neuromere 1 (in the honeybee). © 1998 by The National Academy of Sciences 0027-8424y98y9511290-5$2.00y0 ‡To whom reprint requests should be addressed at: Division of Biology PNAS is available online at www.pnas.org. 216-76, Pasadena, CA 91125. e-mail: [email protected]. 11290 Downloaded by guest on September 26, 2021 Evolution: La Cerra and Bingham Proc. Natl. Acad. Sci. USA 95 (1998) 11291 outbidding, conflicts over the exchange value of commodities, Mammalian Behavioral Intelligence in Phylogenetic and and preference for partners offering the highest value (16, 17). Systematic Perspective They have significantly greater correspondence to most social exchange phenomena than earlier game theoretic conceptu- The sine qua non of behavioral intelligence systems is the alizations, but these models only begin to suggest the multi- capacity to predict the future—to model likely behavioral dimensional, dynamic character of hominid biological markets. outcomes in the service of inclusive fitness. This logic is already An individual can be engaged in numerous cooperative and evident, in a primitive sense, in Escherichia coli: information competitive relationships simultaneously, with one or more transduced by environmental sensors directs behavioral re- other individuals who are themselves concurrently engaged in sponses in a manner that increases the probability of the various cooperative and competitive constellations within the attainment of bioenergetic resources in the next moment (18, same group. Cooperative alliances between individuals can be 19). based on one or more of any number of different commodities Centralized nervous systems are characterized by numerous or services, and a cooperator for the attainment of one goal design features that enhance predictive capacity. An adapta- can be a competitor for another. The intrinsically fluctuating tion found in even the simplest centralized nervous system is nature of critical market variables further increases the com- a region of highly plastic tissue specialized for the purpose of instantiating representations (i.e., neural activation vectors plexity of problem-solving in the market environment. The that convey information). This substrate, acting in concert with value of an individual as a cooperative partner can change the integrated system in which it is situated, allows for the directly as a function of age, injury, pregnancy, the formation y retention of essential information about the probabilistic of new alliances, and or changing cooperative task priorities, relationships between specific sensory inputs, behavioral re- and it can change indirectly as a function of shifting alliances, sponses, and the adaptive value of the outcomes of these power centers, and numerous other perturbations in the behaviors as established by homeostaticylife history regulatory greater market. In the relatively closed biological markets of system components. ancestral hominid populations, a single social behavioral out- Recent work exploring mechanisms of associative learning put, the product of
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