Pheromones enhance somatosensory processing in newt brains through a vasotocin-dependent mechanism

Abstract

We tested whether the sex pheromones that stimulate courtship clasping in male roughskin newts do so, at least in part, by amplifying the somatosensory signals that directly trigger the motor pattern associated with clasping and, if so, whether that amplification is dependent on endogenous vasotocin (VT). Female olfactory stimuli increased the number of action potentials recorded in the medulla of males in response to tactile stimulation of the cloaca, which triggers the clasp motor reflex, as well as to tactile stimulation of the snout and hindlimb. That enhancement was blocked by exposing the medulla to a V1a receptor antagonist before pheromone exposure. However, the antagonist did not affect medullary responses to tactile stimuli in the absence of pheromone exposure, suggesting that pheromones amplify somatosensory signals by inducing endogenous VT release. The ability of VT to couple sensory systems together in response to social stimulation could allow this peptide to induce variable behavioural outcomes, depending on the immediate context of the social interaction and thus on the nature of the associated stimuli that are amplified. If widespread in vertebrates, this mechanism could account for some of the behavioural variability associated with this and related peptides both within and across species.

Figure 1

(a) Diagram of the area where recordings were made (dots indicate representative recording sites), (b) a representative trace of neuronal activity in response to the three different types of somatosensory stimulation as well as (c) a timeline of events during a recording session.

Figure 2

When FSW was applied continuously to the nares for 30 min, the medullary response to cloacal pressure increased across recording intervals during exposure. However, no increase in responsiveness was seen in the animals whose medulla was perfused with Manning compound or in those whose nares were exposed to tap water, regardless of medullary treatment. Mean±s.e.m. of responses to cloacal pressure across recording intervals (a) in animals with saline perfused onto the medulla and FSW applied to the nares, (b) in animals with Manning perfused onto the medulla and FSW applied to the nares, (c) in animals with saline perfused onto the medulla and tap water applied to the nares and (d) in animals with Manning perfused onto the medulla and tap water applied to the nares. ^**Indicates significantly more action potentials than were recorded during baseline conditions prior to olfactory stimulation, p<0.01.

Figure 3

When FSW was applied continuously to the nares for 30 min, the medullary response to snout pressure increased across recording intervals during exposure. However, no increase in responsiveness was seen in the animals whose medulla was perfused with Manning compound or in those whose nares were exposed to tap water, regardless of medullary treatment. Mean±s.e.m. of responses to snout pressure across recording intervals (a) in animals with saline perfused onto the medulla and FSW applied to the nares, (b) in animals with Manning perfused onto the medulla and FSW applied to the nares, (c) in animals with saline perfused onto the medulla and tap water applied to the nares and (d) in animals with Manning perfused onto the medulla and tap water applied to the nares. ^*Indicates significantly more action potentials than were recorded during baseline conditions prior to olfactory stimulation, p<0.05.

Figure 4

When FSW was applied continuously to the nares for 30 min, the medullary response to hindlimb pressure increased across recording intervals during exposure, but more slowly than did cloacal and snout responsiveness. However, no increase in response was seen in the animals whose medulla was perfused with Manning compound or in those whose nares were exposed to tap water, regardless of medullary treatment. Mean±s.e.m. of responses to hindlimb pressure across recording intervals (a) in animals with saline perfused onto the medulla and FSW applied to the nares, (b) in animals with Manning perfused onto the medulla and FSW applied to the nares, (c) in animals with saline perfused onto the medulla and tap water applied to the nares and (d) in animals with Manning perfused onto the medulla and tap water applied to the nares (n=8). ^*Indicates significantly more action potentials than were recorded during baseline conditions prior to olfactory stimulation, p<0.05.