Putting it in Context: Linking Auditory Processing with Social Behavior Circuits in the Vertebrate Brain

Abstract

Context is critical to the adaptive value of communication. Sensory systems such as the auditory system represent an important juncture at which information on physiological state or social valence can be added to communicative information. However, the neural pathways that convey context to the auditory system are not well understood. The serotonergic system offers an excellent model to address these types of questions. Serotonin fluctuates in the mouse inferior colliculus (IC), an auditory midbrain region important for species-specific vocalizations, during specific social and non-social contexts. Furthermore, serotonin is an indicator of the valence of event-based changes within individual social interactions. We propose a model in which the brain's social behavior network serves as an afferent effector of the serotonergic dorsal raphe nucleus in order to gate contextual release of serotonin in the IC. Specifically, discrete vasopressinergic nuclei within the hypothalamus and extended amygdala that project to the dorsal raphe are functionally engaged during contexts in which serotonin fluctuates in the IC. Since serotonin strongly influences the responses of IC neurons to social vocalizations, this pathway could serve as a feedback loop whereby integrative social centers modulate their own sources of input. The end result of this feedback would be to produce a process that is geared, from sensory input to motor output, toward responding appropriately to a dynamic external world.

Fig. 1

The emergence of contextual state. An animal’s contextual state is established by a complex interaction between internal physiology, environmental conditions, and the neural circuitry sensitive to both.

Fig. 2

Serotonergic increases within the IC are dependent on specific external events. Of the five non-social conditions tested, only the presentation of noise and the restriction of movement within a cylindrical arena significantly increased serotonin relative to no stimulus. Figure adapted from Hall etal. 2010, J Exp Bio 213:1009–1017.

Fig. 3

Serotonin in the IC parallels the valence of social interactions for males interacting with females. (A) Females squeak at low levels in the initial phase of interactions that proceed to mounting (light bars), but at high levels in the initial phase of interactions that do not proceed to mounting (gray bars). (B) Serotonin increases in the IC of males following the presentation of novel female partners (“interaction”) as opposed to no partner (“control”). (C) The amplitude of increases in serotonin correlate inversely with the number of female squeaks. Figures adapted from Finton etal. 2017, Anim Behav 126:163–175 (A) and Keesom and Hurley 2016, J Neurophysiol 115:1786–1796 (B, C).

Fig. 4

Model of context-dependent feedback from the SBN to the inferior colliculus, through the dorsal raphe nucleus. AVP-positive neurons in the PVN and BNST respond to threatening or social events, and subsequently influence firing rates of neurons in the dorsal raphe nucleus, which release serotonin in sensory regions like the IC. Modulation of firing patterns of IC neurons by serotonin could in turn alter ascending sensory information.