Effects of amygdala lesions on male mouse ultrasonic vocalizations and copulatory behaviour

Graduate School of Arts and Sciences, The University of Tokyo, Japan.
Neuroreport (Impact Factor: 1.52). 06/2012; 23(11):676-80. DOI: 10.1097/WNR.0b013e3283557eea
Source: PubMed


Mice produce ultrasonic vocalizations (USVs) in several behavioural contexts. In particular, male mice articulate a long series of various sounds to females during courtship behaviour. To determine the relationships between this kind of vocal behaviour and emotion, we examined the lesion effects of the amygdala, an important neural module in emotional behaviour, on USVs. We recorded USVs from mice in the lesion and the control (sham operation) groups upon presentation of females and compared USVs before and after surgery. We found that the mean syllable duration of the USVs shortened and the appearance rate of longer syllables decreased after the surgery. The main reasons for these alterations could be explained by the altered courtship behaviour. As reported previously, the mounting behaviour of the lesion group after surgery was markedly less than that of the control group. Therefore, the appearance rate of those longer syllables would decrease logically because longer syllables primarily appear during mounting and intromission. However, we can hypothesize another scenario for the alterations to vocal behaviour: effects on the direct amygdala-periaqueductal grey (PAG) projection might be involved in the increase in the appearance rate of shorter syllables owing to lesion-induced loss of emotions, such as vigilance. Overall, the results suggested two possible mechanisms of the amygdala lesions on the alteration of the vocal behaviour.

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    • "Based upon changes in USVs reported in several genetic models of autism, which may reflect a similar spectrum of social deficits to that seen after pediatric TBI [26], [29], [35], [36], [37], we hypothesized that injury to the developing brain would also result in altered vocalizations in a social or sociosexual context. Only one other study to date has considered USVs in the context of a mechanical brain injury - Matsumoto and colleagues demonstrated that direct bilateral lesions of the amygdala in adult male mice reduced syllable duration and long syllable frequency, which corresponded to a reduction in mounting behavior in the same mice [94]. "
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    ABSTRACT: Despite the life-long implications of social and communication dysfunction after pediatric traumatic brain injury, there is a poor understanding of these deficits in terms of their developmental trajectory and underlying mechanisms. In a well-characterized murine model of pediatric brain injury, we recently demonstrated that pronounced deficits in social interactions emerge across maturation to adulthood after injury at postnatal day (p) 21, approximating a toddler-aged child. Extending these findings, we here hypothesized that these social deficits are dependent upon brain maturation at the time of injury, and coincide with abnormal sociosexual behaviors and communication. Age-dependent vulnerability of the developing brain to social deficits was addressed by comparing behavioral and neuroanatomical outcomes in mice injured at either a pediatric age (p21) or during adolescence (p35). Sociosexual behaviors including social investigation and mounting were evaluated in a resident-intruder paradigm at adulthood. These outcomes were complemented by assays of urine scent marking and ultrasonic vocalizations as indices of social communication. We provide evidence of sociosexual deficits after brain injury at p21, which manifest as reduced mounting behavior and scent marking towards an unfamiliar female at adulthood. In contrast, with the exception of the loss of social recognition in a three-chamber social approach task, mice that received TBI at adolescence were remarkably resilient to social deficits at adulthood. Increased emission of ultrasonic vocalizations (USVs) as well as preferential emission of high frequency USVs after injury was dependent upon both the stimulus and prior social experience. Contrary to the hypothesis that changes in white matter volume may underlie social dysfunction, injury at both p21 and p35 resulted in a similar degree of atrophy of the corpus callosum by adulthood. However, loss of hippocampal tissue was greater after p21 compared to p35 injury, suggesting that a longer period of lesion progression or differences in the kinetics of secondary pathogenesis after p21 injury may contribute to observed behavioral differences. Together, these findings indicate vulnerability of the developing brain to social dysfunction, and suggest that a younger age-at-insult results in poorer social and sociosexual outcomes.
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    ABSTRACT: Vocalizations transmit information to social partners, and mice use these signals to exchange information during courtship. Ultrasonic vocalizations from adult males are tightly associated with their interactions with females, and vary as a function of male quality. Work in the last decade has established that the spectrotemporal features of male vocalizations are not learned, but that female attention toward specific vocal features is modified by social experience. Additionally, progress has been made on elucidating how mouse vocalizations are encoded in the auditory system, and on the olfactory circuits that trigger their production. Together these findings provide us with important insights into how vocal communication can contribute to social interactions.
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