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. 2016 Sep 20;10:399.
doi: 10.3389/fnins.2016.00399. eCollection 2016.

Amygdalar Auditory Neurons Contribute to Self-Other Distinction During Ultrasonic Social Vocalization in Rats

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Free PMC article

Amygdalar Auditory Neurons Contribute to Self-Other Distinction During Ultrasonic Social Vocalization in Rats

Jumpei Matsumoto et al. Front Neurosci. .
Free PMC article

Abstract

Although, clinical studies reported hyperactivation of the auditory system and amygdala in patients with auditory hallucinations (hearing others' but not one's own voice, independent of any external stimulus), neural mechanisms of self/other attribution is not well understood. We recorded neuronal responses in the dorsal amygdala including the lateral amygdaloid nucleus to ultrasonic vocalization (USVs) emitted by subjects and conspecifics during free social interaction in 16 adult male rats. The animals emitting the USVs were identified by EMG recordings. One-quarter of the amygdalar neurons (15/60) responded to 50 kHz calls by the subject and/or conspecifics. Among the responsive neurons, most neurons (Type-Other neurons; 73%, 11/15) responded only to calls by conspecifics but not subjects. Two Type-Self neurons (13%, 2/15) responded to calls by the subject but not those by conspecifics, although their response selectivity to subjects vs. conspecifics was lower than that of Type-Other neurons. The remaining two neurons (13%) responded to calls by both the subject and conspecifics. Furthermore, population coding of the amygdalar neurons represented distinction of subject vs. conspecific calls. The present results provide the first neurophysiological evidence that the amygdala discriminately represents affective social calls by subject and conspecifics. These findings suggest that the amygdala is an important brain region for self/other attribution. Furthermore, pathological activation of the amygdala, where Type-Other neurons predominate, could induce external misattribution of percepts of vocalization.

Keywords: amygdala; auditory hallucination; self/other attribution; single unit recording; ultrasonic vocalization.

Figures

Figure 1
Figure 1
Waveform characteristics of two representative amygdala neurons. (A) Waveforms (mean ± SD, shaded) simultaneously recorded from the four tetrode leads (EL 1–4). The waveforms indicated by a and b correspond to the two clusters in (B). (B) The results of an offline cluster analysis. Each dot represents one spike. The horizontal axis represents the first principle component (PC 1) of EL 2, and the vertical axis represents PC 1 of EL 4. (C) Autocorrelograms of neurons a and b. Autocorrelograms of neurons a and b show that refractory periods of the neurons were greater than 2 ms, consistent with these spikes originating from single neurons. Bin width = 1 ms.
Figure 2
Figure 2
Fifty kilohertz calls and TA EMG. (A) Examples of simultaneously recorded sonograms and TA EMGs acquired during recording sessions where subjects interacted with devocalized female rats (DF sessions) [left: a call with limited range frequency modulation (non-WFM call); right; a call with wide range frequency modulation (WFM call)]. (B) In a representative DF session, the relation between the range of frequency modulation (FM range) of 50-kHz calls and the maximum EMG amplitude around the calls. Each point represents a call. (C) The distribution of frequency modulation ranges of high frequency calls of all DF sessions. White bars: calls with frequency modulation < 15 kHz (non-WFM calls); gray bars: calls with frequency modulation >15 kHz (WFM calls). Error bar: SEM. (D) The percentage of all non-WFM and WFM calls emitted with clear EMG activity (maximum amplitude >3) over all DF sessions. Error bar: SEM. *** signifies p < 0.001, paired t-test.
Figure 3
Figure 3
Assignment of WFM calls during social interactions between vocalizing male rats (M sessions). (A) An example of call assignment. Simultaneously recorded sonogram (top), TA EMG of a subject rat (middle), and TA EMG of a stimulus conspecific (bottom) are shown. Each rectangle demarcated by dashed lines in the sonogram represents one call and the color of the square represents estimated source of the call (blue: the subject rat; red: the stimulus rat; black: indistinguishable) based on the concurrent TA EMG. Sub: subject; Stim: stimulus rat. (B) Distribution of call assignments. (C,D) Averaged (horizontal plane) speeds measured from the trunks (C) of and the head (translation) relative to the trunk (D). Speeds are shown for the call-emitting (blue) and non-emitting (red) rats. The solid lines and translucent areas indicate the means and SEMs, respectively. Time zero represents the onset of the calls. (E,F) The change in trunk speed in horizontal plane and head movement relative to the trunk around the onset of WFM calls [Δspeed around onset = (mean speed during the first 0.5 s after call onset) − (mean speed at −1.0 to −0.5 s prior to call onset)] of either the call-emitting (blue) or non-emitting (red) rats. (*** indicates p < 0.001, paired t-test). (G) The change in head movement relative to trunk after the onset of WFM calls [Δspeed after onset = (mean speed at 0.35–0.45 s after call onset) − (mean speed at −0.1–0.0 s prior to call onset)] of the non-emitting rats. (## signifies p < 0.01, one-sample t-test).
Figure 4
Figure 4
Single unit activity during WFM calls by the conspecific and the subject in M sessions. (A–C) Perievent rasters and histograms of three neurons (A) an excitatory Type-Other neuron; (B) an inhibitory Type-Other neuron; (C) an excitatory Type-Both neuron. Bin widths = 40 ms. Time zero represents onset of the call. Each number (n) at the top right of the panel indicates the number of calls analyzed. Gray shading indicates the call durations. (D) The response selectivity (selectivity index, SI) of Type-Other and Type-Self neurons. The dashed line indicates the expected value if responses to the WFM calls by the conspecific and subject were equal. #, significantly different from the expected value, p < 0.05, Wilcoxon signed rank test; +, tendency of the difference between Type-Other and Type-Self neurons, p < 0.1, Wilcoxon rank sum test.
Figure 5
Figure 5
Neuronal activity and rats' motion around the randomly shifted call onsets. (A–C) Peri-event histograms of spike activity around the randomly shifted call onsets (filled bars) of neurons shown in Figures 4A–C, respectively. Dotted lines indicate original responses. Responses to the call by the conspecific (pink) are displayed above and those of the subject (blue) below. (D,E) Average running (D) and head movement (E) speeds of interacting male subject and conspecific rats (30 rats; 27 M sessions) around the randomly shifted call onsets by the call-emitting (light blue) and non-emitting (pink) rats and the original data before the random shift (dotted line). The other descriptions are the same as those for Figures 3C,D. (F,G) The change in running speed and head movement around the randomly shifted onsets (left; light blue and pink) and original ones (right; blue and red) of either the call-emitting (light blue/blue) or non-emitting (pink/red) rats. Note that the speeds at the different onsets showed no significant difference (paired t-test, p > 0.05). Other descriptions are the same as those for Figures 3E,F. (H) Comparison of head movement after the random-shifted onsets (left) and original ones (right) of the non-emitting rats. The speed changes for the different onsets were not significantly different (paired t-test between the data before and after the random shift, p > 0.05). Other descriptions are the same as those for Figure 3G.
Figure 6
Figure 6
Recording site histological analyses. Positions of Type-Other, Type-Self, and Type-Both neurons are represented by red, blue, and black symbols, respectively. The inset keys indicate response types. Gray dots represent positions of non-responsive neurons. The value below each section indicates distance (mm) from bregma. L, lateral amygdaloid nucleus; BL, basolateral amygdaloid nucleus; BM, basomedial amygdaloid nucleus; M, medial amygdaloid nucleus; C, central amygdaloid nucleus; LV, lateral ventricle. The atlas diagrams were adapted from Paxinos and Watson (2006) with permission.

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