Basolateral amygdala responds robustly to social calls: spiking characteristics of single unit activity

Abstract

Vocalizations emitted within a social context can trigger call-specific changes in the emotional and physiological/autonomic state of the receiver. The amygdala is implicated in mediating these changes, but its role in call perception remains relatively unexplored. We examined call and pitch selectivity of single neurons within the basolateral amygdala (BLA) by recording spiking activity in response to 5 pitch variants of each of 14 species-specific calls presented to awake, head-restrained mustached bats, Pteronotus parnellii. A response-wise analysis across neurons revealed seven types of temporal response patterns based on the timing and duration of spiking. Roughly half of the responses to different call types were significantly affected by changes in call pitch. A neuron-wise analysis revealed that ∼ 12% (8/69) of the neurons preferred the same pitch across all call types. Ninety-three percent (93/100) of neurons were excited by at least one call type and 76% exhibited either complete or transient suppression to one or more call types. The majority of neurons preferred fewer than half of the 14 different simple-syllabic calls. A call-wise analysis of spiking activity revealed that call types signaling either threat or fear most consistently evoked increases in the spike rate. In contrast, calls emitted during appeasement tended to evoke spike suppression. Our data suggest that BLA neurons participate in the processing of multiple call types and exhibit a rich variety of temporal response patterns that are neither neuron nor call specific.

Auditory Responses to Vocal Sounds in the Songbird Nucleus Taeniae of the Amygdala and the Adjacent Arcopallium

“…The ratio of stimulus-selective cells to all recorded cells was larger in the surrounding arcopallium (34.1%) than in the TnA (20.3%), suggesting that neurons in this area can represent behavioral relevance of stimuli and be involved in recognizing vocalizations and controlling successive behaviors. Recently, neural activity in the amygdala, especially in the lateral or basolateral subdivision, has been investigated in rodents and bats [Naumann and Kanwal, 2011;Gadziola et al, 2012Gadziola et al, , 2016Parsana et al, 2012;Peterson and Wenstrup, 2012;Grimsley et al, 2013]. In the rat lateral amygdala, it has been known that neurons respond to the cue tones in the fear conditioning [LeDoux et al, 1990].…”

“…Grimsley et al [2013] demonstrated that neurons in the mouse basolateral amygdala are activated when listening to behaviorally aversive vocalizations and that the activity is modulated by visual cues associated with predation. In bats, the neurons in the lateral [Gadziola et al, 2012] or basolateral amygdala [Naumann and Kanwal, 2011;Peterson and Wenstrup, 2012;Gadziola et al, 2016] respond selectively to specific social calls. Subdivision structures and corresponding function in the avian amygdala may not necessarily have evolved the same way as those of mammals.…”

A novel coding mechanism for social vocalizations in the lateral amygdala

“…The present study assessed response duration using two different measures. The first measure used a sliding 20-ms average of the PSTH to analyze response duration across a block of trials, a method commonly used for assessing response duration (Bendor and Wang 2008;Naumann and Kanwal 2011). Although derived, this type of measure uses confidence intervals to take into account the trial-by-trial variance, and it provides a more faithful representation of the original raster data.…”

“…In studies of basolateral amygdalar responses, persistent firing is observed in auditory and other sensory stimuli (Bordi and LeDoux 1992;Bordi et al 1993;Maeda et al 1992;Naumann and Kanwal 2011) but is generally not characterized. Our results show that persistent firing in the lateral amygdala has the potential to carry discriminatory information for coding social vocalizations at the single-neuron level and that duration of persistent firing carried more information for discriminating among social vocalizations than firing rate.…”

“…Inspection of their results reveals that persistent firing responses are present in the basolateral amygdala and may be more common during awake conditions, supporting the idea that the behavioral state of the animal may be a critical factor driving persistent firing. In awake, mustached bats (Pteronotus parnellii), basolateral amygdalar responses appear more selective for particular social vocalizations than in big brown bats (Naumann and Kanwal 2011;Peterson and Wenstrup 2008), with persistent firing commonly observed in response to a highly aggressive vocalization (Peterson and Wenstrup 2008). Although the significance of persistent firing during passive auditory processing remains unclear, our finding that social vocalizations related to aggression are more likely to evoke persistent firing and our observations of persistent firing in Figs.…”