A neurochemical hypothesis for the origin of hominids

Abstract

It has always been difficult to account for the evolution of certain human characters such as language, empathy, and altruism via individual reproductive success. However, the striatum, a subcortical region originally thought to be exclusively motor, is now known to contribute to social behaviors and "personality styles" that may link such complexities with natural selection. We here report that the human striatum exhibits a unique neurochemical profile that differs dramatically from those of other primates. The human signature of elevated striatal dopamine, serotonin, and neuropeptide Y, coupled with lowered acetylcholine, systematically favors externally driven behavior and greatly amplifies sensitivity to social cues that promote social conformity, empathy, and altruism. We propose that selection induced an initial form of this profile in early hominids, which increased their affiliative behavior, and that this shift either preceded or accompanied the adoption of bipedality and elimination of the sectorial canine. We further hypothesize that these changes were critical for increased individual fitness and promoted the adoption of social monogamy, which progressively increased cooperation as well as a dependence on tradition-based cultural transmission. These eventually facilitated the acquisition of language by elevating the reproductive advantage afforded those most sensitive to social cues.

Keywords: Ardipithecus; basal ganglia; dopamine; hominin; neurotransmitter.

Fig. 1.

Nissl-stained coronal section from the left hemisphere of a chimpanzee showing the regions sampled for neurotransmitter densities. Those regions included the dorsal caudate nucleus (dC), medial caudate nucleus (mC), and dorsal putamen (dP). C, caudate nucleus; cc, corpus callosum; ic, internal capsule; P, putamen; vS, ventral striatum. To the left of the Nissl-stained image is a tracing of a chimpanzee brain, with a dotted line indicating the approximate level of the coronal section.

Fig. 2.

The neurochemical profile of each species within the caudate nucleus [dorsal caudate nucleus (A) and medial caudate nucleus (B)] and putamen (C) for capuchin, pig-tailed macaque, olive baboon, gorilla, chimpanzee, and human. NPY (green box plots) and 5HT transporter (red box plots) data are from the present study and are shown in SI Appendix, Fig. S1. ACh data (as measured by choline acetyltransferase-immunoreactive axons; beige box plots) are from ref. , and DA (as measured by TH-immunoreactive axons; white box plots) are from ref. . Dopaminergic innervation was highest in human medial caudate nucleus, the striatal region involved in social reward, and humans are the only species to have higher DA relative to ACh content in all three striatal sampling regions. Interestingly, DA within the human medial caudate nucleus was consistently high, with little interindividual variation. ACh was elevated in humans and apes, but humans possessed lower concentrations relative to the apes. Asterisks indicate outliers.

Fig. 3.

Role of striatum neurochemistry in human origins. As primates moved from an r-to K-life history strategy, striatal 5HT levels increased to buffer against aggression and striatal NPY levels also rose, at least in some species, to facilitate increased social competence. In our sample, humans, chimpanzees, and gorillas show increased 5HT relative to other primates within sampled striatal regions, and humans and chimpanzees also share increased NPY. Extant apes now exhibit high striatal cholinergic innervation and low DA, a combination that is associated with personality styles that are externally motivated and characterized by aggressiveness, dominance, low motivation to alter ongoing behaviors in response to social or environmental stimuli, as well as a relatively superficial knowledge of the environment. In contrast, humans now possess high striatal DA and low ACh innervation, a unique profile that is accompanied by increased externally motivated behaviors. The human profile is associated with conformity behaviors that are more responsive to social and environmental cues, decreased aggression, and a more sophisticated knowledge of the environment. High concentrations of striatal DA are also associated with pair bonds (i.e., monogamy). The progressive evolution of increasing DA combined with decreasing ACh (to reduce aggression) accounts for why humans can display social, rather than territorial, monogamy. We posit that an earlier manifestation of this profile was central to the success of human ancestors and helped initiate social monogamy in post-LCA hominids.

Fig. 4.

Extraordinary characters in earliest known hominids. Ardipithecus displays evidence of the simultaneous elimination of the sectorial canine complex and adoption of upright walking. Its likely descendant, Australopithecus, exhibits unusual demographic success (15). As outlined here, each of these is strikingly consistent with pivotal changes in the cortico-striatal reward pathway and striatum (Fig. 3). Although our knowledge is still incomplete, some elements of the human reward pathway are similar to those of primates that pair-bond, and such primates are typically territorial. However, early hominids were omnivores relying substantially on lower canopy/terrestrial resources. Territoriality like that either of chimpanzees (ripe fruit frugivores defending upper canopy patches) or gorillas (relying on continuously distributed terrestrial herbaceous vegetation) would have been strategically unsustainable for hominids. Terrestrial collection sectors would have been too large for aggressive defense because of their requisite search-intensive food strategy, and broad searches would have been hazardous for females with dependent offspring. However, habitual male copulations with individual females in exchange for collected protein-rich food items (provisioning), as occasionally seen in extant chimpanzees, could have dramatically increased male paternity and enhanced subadult and female survivorship. The changes in basal ganglia neurochemistry shown here would have allowed multiple pair-bonds to coexist within a single social group. Other aspects of a DDS personality type would have increased habitat awareness, which is critical for food location and predator evasion. Under such conditions, selection would have favored male choice of females whose ovulatory status remained cryptic, especially if it included a simulation of lactational amenorrhea (noncyclicly enlarged mammary glands). The breakthrough adaptation of early hominids was therefore likely dependent upon multiple modifications in the basal ganglia that could promote social (nonterritorial) monogamy.