Sex Steroids as Regulators of Gestural Communication

Abstract

Gestural communication is ubiquitous throughout the animal kingdom, occurring in species that range from humans to arthropods. Individuals produce gestural signals when their nervous system triggers the production of limb and body movement, which in turn functions to help mediate communication between or among individuals. Like many stereotyped motor patterns, the probability of a gestural display in a given social context can be modulated by sex steroid hormones. Here, we review how steroid hormones mediate the neural mechanisms that underly gestural communication in humans and nonhumans alike. This is a growing area of research, and thus we explore how sex steroids mediate brain areas involved in language production, social behavior, and motor performance. We also examine the way that sex steroids can regulate behavioral output by acting in the periphery via skeletal muscle. Altogether, we outline a new avenue of behavioral endocrinology research that aims to uncover the hormonal basis for one of the most common modes of communication among animals on Earth.

Figure 1.

Examples of gestures in vertebrates. (A) A gesture associated with surprise in humans. This photograph was used by Charles Darwin in his book, The Expression of the Emotions in Man and Animals [(114); licensed under Getty Museum Open Content Program]. (B) A territorial gesture of hippopotamus [Hippopotamus amphibious (115); credit: Robert A. Tobiansky, with permission]. (C) A mating gesture from a male Victoria’s riflebird (Ptiloris victoriae), whereby he hold out his wings and move his head side-to-side (31) (credit: Francesco Veronesi licensed under CC BY-SA 2.0). (D) A Bornean rock frog (Staurois parvus) producing a foot-flagging gesture to compete with rival males at a breeding site [(116); credit: Vienna Zoo/Doris Preininger, with permission]. (E) A male peacock spider (Maratus splendens) performing a mating display in which it raises its abdomen and waves its hind legs [(117); credit: Jurgen Otto licensed under CC BY-NC-ND 2.0]. (F) A springbok (Antidorcas marsupialis) performing a stotting display, in which it leaps into the air to notify predators that they have been detected [ (118); credit: Yathin sk licensed under CC BY-SA 3.0]). (G) A male white-collared manakin (Manacus manacus) in a “beard up” posture, which typically occurs when the male is dancing for the female [ (65); credit: Steve Garvie licensed under CC BY-NC-SA 2.0]. (H) A male brown anole (Anolis sagrei) gestures to conspecifics and potential predators by extending its dewlap (orange throat patch) in a rhythmic pattern [(119) credit: touterse, licensed under CC BY 2.0].

Figure 2.

Neural nodes associated with co-speech gesture and other forms of gesture (eg, pantomime) in humans. Neural nodes associated with co-speech gesture (white or gray) include the premotor cortex (PM), hippocampus (HPC), parahippocampal cortex (PHC), left inferior frontal gyrus (IFG), anterior superior temporal gyrus, (ASTG), and bilateral posterior superior temporal sulcus (PSTS). Neural associated with other forms of gesture (eg, pantomime) (black) include the PM, areas of the middle frontal gyrus (MFG), posterior parietal cortex (PPC), the primary motor cortex (M1), and the posterior medial temporal cortex (PMT). The PM is shaded gray to signify its role in both co-speech and gesture.

Figure 3.

Regions of evolutionary conserved social decision-making network and its interaction with the gesture/co-speech gesture network in the human brain. Select nodes of the social decision making network (red), which include areas from the social behavior network and the motivational/reward circuit (described by 50). Regions involved in co-speech gesture and other forms of gesture (eg, pantomime) are shaded in gray. Nodes that act as an interface between the social decision making network and co-speech/gestural networks a shaded with a gray-red gradient (ie, “Both networks”). Abbreviations: AH, anterior hypothalamus; AMY, amygdala; BNST, bed nucleus of the stria terminalis, HPC, hippocampus; ICo, intercollicular nucleus; M1, primary motor cortex; mPFC, medial prefrontal cortex; mPOA, medial preoptic area; NAc, nucleus accumbens; NRA, nucleus retroambiguus; PAG, periaqueductal gray; RAm, nucleus retroambigualis; VMH, ventromedial hypothalamus; VP, ventral pallidum; VTA, ventral tegmental area.