Forward shift of feeding buzz components of dolphins and belugas during associative learning reveals a likely connection to reward expectation, pleasure and brain dopamine activation

Abstract

For many years, we heard sounds associated with reward from dolphins and belugas. We named these pulsed sounds victory squeals (VS), as they remind us of a child's squeal of delight. Here we put these sounds in context with natural and learned behavior. Like bats, echolocating cetaceans produce feeding buzzes as they approach and catch prey. Unlike bats, cetaceans continue their feeding buzzes after prey capture and the after portion is what we call the VS. Prior to training (or conditioning), the VS comes after the fish reward; with repeated trials it moves to before the reward. During training, we use a whistle or other sound to signal a correct response by the animal. This sound signal, named a secondary reinforcer (SR), leads to the primary reinforcer, fish. Trainers usually name their whistle or other SR a bridge, as it bridges the time gap between the correct response and reward delivery. During learning, the SR becomes associated with reward and the VS comes after the SR rather than after the fish. By following the SR, the VS confirms that the animal expects a reward. Results of early brain stimulation work suggest to us that SR stimulates brain dopamine release, which leads to the VS. Although there are no direct studies of dopamine release in cetaceans, we found that the timing of our VS is consistent with a response after dopamine release. We compared trained vocal responses to auditory stimuli with VS responses to SR sounds. Auditory stimuli that did not signal reward resulted in faster responses by a mean of 151 ms for dolphins and 250 ms for belugas. In laboratory animals, there is a 100 to 200 ms delay for dopamine release. VS delay in our animals is similar and consistent with vocalization after dopamine release. Our novel observation suggests that the dopamine reward system is active in cetacean brains.

Buzzing during biosonar-based interception of prey in the delphinids Tursiops truncatus and Pseudorca crassidens

“…These were short click trains of low (~2 ms for BJ and 2-5 ms for Kina), nearly constant or slightly increasing ICIs (Fig. 1) that may be analogous to the recently described victory squeals (VS) produced by trained belugas and bottlenose dolphins elsewhere (Ridgway et al, 2014). Because of their post-capture occurrence and their apparent communicative, rather than echolocation, function, the VS were disregarded in further ICI analyses (e.g.…”

“…However, it was not until the development of sound recording tags that this interpretation could be substantiated. It is now clear that buzzes are associated with prey capture attempts in sperm whales (Miller et al, 2004), beaked whales , pilot whales (Aguilar Soto et al, 2008), porpoises (DeRuiter et al, 2009) and belugas (Ridgway et al, 2014).…”

Variation in the emission rate of sounds in a captive group of false killer whales Pseudorca crassidens during feedings: possible food anticipatory vocal activity?

“…Moreover, the fi sh tossed into the tank might have developed competition among the animals with an increase in production of burst pulses (Overstrom, 1983;Connor and Smolker, 1996;Herzing, 1996;Lammers et al, 2003;Nowacek, 2005). Moreover, Ridgway et al (2014) suggested that burst pulses produced during feeding sessions might be considered as food calls with emotional content. Nevertheless, more substantial experiments involving the diff erent aspects of food delivery should be carried out (food quantity and quality, hunger levels, and interaction with the keepers) (Dittus, 1984;Caine at al., 1995;Di Bitetti, 2005;Slocombe and Zuberbühler, 2006;Clay and Zuberbühler, 2009) to assess the presence of a referential content in the calls of dolphins ( Ralston and Herman, 1989 ;Herzing, 2000;Akiyama and Ohta, 2007;Therrien et al, 2012).…”

On doing two things at once: dolphin brain and nose coordinate sonar clicks, buzzes, and emotional squeals with social sounds during fish capture

“…As they hunt for fish, the complex, asymmetrical, muscular nose makes brief, high-peak frequency click trains that are focused through the fatty melon-shaped forehead (Au, 1993;Jensen et al, 2009;Ridgway et al, 2014;Wisniewska et al, 2014). The clicks bounce off fish, returning echoes to the dolphin's ear (Au, 1993) where the cochlea converts the echoes into nerve impulses (McCormick et al, 1970(McCormick et al, , 1980.…”

“…The first two phases of fish capture, sonar clicking and the terminal buzz (TB), have received a good deal of attention in T. truncatus and other cetaceans (Au et al, 2013;Wisniewska et al, 2014). The victory squeal (VS) is a third phase (Ridgway et al, 2014). This third phase has not received as much attention with respect to fish capture.…”