Communication calls produced by electrical stimulation of four structures in the guinea pig brain

Abstract

One of the main central processes affecting the cortical representation of conspecific vocalizations is the collateral output from the extended motor system for call generation. Before starting to study this interaction we sought to compare the characteristics of calls produced by stimulating four different parts of the brain in guinea pigs (Cavia porcellus). By using anaesthetised animals we were able to reposition electrodes without distressing the animals. Trains of 100 electrical pulses were used to stimulate the midbrain periaqueductal grey (PAG), hypothalamus, amygdala, and anterior cingulate cortex (ACC). Each structure produced a similar range of calls, but in significantly different proportions. Two of the spontaneous calls (chirrup and purr) were never produced by electrical stimulation and although we identified versions of chutter, durr and tooth chatter, they differed significantly from our natural call templates. However, we were routinely able to elicit seven other identifiable calls. All seven calls were produced both during the 1.6 s period of stimulation and subsequently in a period which could last for more than a minute. A single stimulation site could produce four or five different calls, but the amygdala was much less likely to produce a scream, whistle or rising whistle than any of the other structures. These three high-frequency calls were more likely to be produced by females than males. There were also differences in the timing of the call production with the amygdala primarily producing calls during the electrical stimulation and the hypothalamus mainly producing calls after the electrical stimulation. For all four structures a significantly higher stimulation current was required in males than females. We conclude that all four structures can be stimulated to produce fictive vocalizations that should be useful in studying the relationship between the vocal motor system and cortical sensory representation.

Involvement of rat posterior prelimbic and cingulate area 2 in vocalization control

“…Our data confirm and greatly extend earlier evidence that pointed to a role of rodent prefrontal cortex in vocalization control. Such earlier data include, scattered vocalizations evoked by electric stimulation in rat frontal cortex (Burgdorf et al., ), responses to vocalizations in rat anterior cingulate cortex (Saito & Okanoya, ), vocalizations evoked by electric stimulation in the frontal cortex of anesthetized guinea pigs (Green et al., ) and the abolition of fear calls by lesions to frontal cortex (Frysztak & Neafsey, ). It appears that electrically evoked calls were more common in our study than in previous work.…”

“…It appears that electrically evoked calls were more common in our study than in previous work. The higher incidence of vocalization might be related to the fact that we applied the stimulation in awake rather than anesthetized animals (Green et al., ) and that we applied higher current intensities (Burgdorf et al., ). A potential limitation of our microstimulation work is the use of head‐fixation, a procedure stressful to the experimental animals, which may have also altered the animal's calling behavior.…”

“…Frysztak and Neafsey provided lesion evidence for an involvement of infralimbic cortex in the control of alarm calls emitted in an aversive conditioning paradigm (Frysztak & Neafsey, ). Recently, the vocal abilities of rodents found more attention both as indices of emotional processing (Knutson, Burgdorf, & Panksepp, ; Wöhr & Schwarting, ) and in the context of courtship (Arriaga, Zhou, & Jarvis, ) and microstimulation work in anesthetized guinea pigs observed vocalizations evoked from medial prefrontal areas (Green et al., ).…”

Circuit and synaptic organization of forebrain-to-midbrain pathways that promote and suppress vocalization

“…Work from the last five decades has established the midbrain periaqueductal gray (PAG) as an obligatory gate for the production of vocalizations in all mammals (Fenzl and Schuller, 2002;Jurgens, 1994Jurgens, , 2002Jurgens, , 2009Subramanian et al, 2020;Sugiyama et al, 2010;Tschida, 2019), and it is thought that forebrain inputs to the PAG regulate the production of vocalizations in a context-dependent fashion. In line with this idea, forebrain regions including the cortex, amygdala, and hypothalamus have been implicated in regulating vocalization as a function of social context (Bennett et al, 2019;Dujardin and Jurgens, 2006;Gao et al, 2019;Green et al, 2018;Jurgens, 1982Jurgens, , 2002Kyuhou and Gemba, 1998;Ma and Kanwal, 2014;Manteuffel et al, 2007). Notably, although electrical or pharmacological activation of various forebrain regions can elicit vocalizations (Jurgens, 2009;Jurgens and Ploog, 1970;Jurgens and Richter, 1986), these effects depend on an intact PAG (Jurgens and Pratt, 1979;Lu and Jurgens, 1993;Siebert and Jurgens, 2003), suggesting that the PAG acts as an essential hub for descending forebrain control of vocalization.…”

Circuit and synaptic organization of forebrain-to-midbrain pathways that promote and suppress vocalization

“…Work from the last five decades has 30 established the midbrain periaqueductal gray (PAG) as an obligatory gate for the production of 31 vocalizations in all mammals (Jurgens, 1994(Jurgens, , 2002(Jurgens, , 2009, and it is thought that forebrain inputs 32 to the PAG regulate the production of vocalizations in a context-dependent fashion. In line with 33 this idea, forebrain regions including the anterior cingulate cortex, amygdala, and hypothalamus 34 have been implicated in regulating vocalization as a function of social context (Bennett et al,35 2019; Dujardin and Jurgens, 2006;Gao et al, 2019;Green et al, 2018;Jurgens, 1982Jurgens, , 200236 Kyuhou and Gemba, 1998; Ma and Kanwal, 2014;Manteuffel et al, 2007). Notably, although 37 electrical or pharmacological activation of a variety of forebrain regions can elicit vocalization 38 (Jurgens, 2009;Jurgens and Ploog, 1970;Jurgens and Richter, 1986), these effects depends 39 on an intact PAG (Jurgens and Pratt, 1979;Lu and Jurgens, 1993;Siebert and Jurgens, 2003), 40…”