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. 2015 May 1;9:102.
doi: 10.3389/fnbeh.2015.00102. eCollection 2015.

Pro-social 50-kHz Ultrasonic Communication in Rats: Post-Weaning but Not Post-Adolescent Social Isolation Leads to Social Impairments-Phenotypic Rescue by Re-Socialization

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Pro-social 50-kHz Ultrasonic Communication in Rats: Post-Weaning but Not Post-Adolescent Social Isolation Leads to Social Impairments-Phenotypic Rescue by Re-Socialization

Dominik Seffer et al. Front Behav Neurosci. .
Free PMC article

Abstract

Rats are highly social animals and social play during adolescence has an important role for social development, hence post-weaning social isolation is widely used to study the adverse effects of juvenile social deprivation and to induce behavioral phenotypes relevant to neuropsychiatric disorders, like schizophrenia. Communication is an important component of the rat's social behavior repertoire, with ultrasonic vocalizations (USV) serving as situation-dependent affective signals. High-frequency 50-kHz USV occur in appetitive situations and induce approach behavior, supporting the notion that they serve as social contact calls; however, post-weaning isolation effects on the behavioral changes displayed by the receiver in response to USV have yet to be studied. We therefore investigated the impact of post-weaning isolation on socio-affective information processing as assessed by means of our established 50-kHz USV radial maze playback paradigm. We showed that post-weaning social isolation specifically affected the behavioral response to playback of pro-social 50-kHz but not alarm 22-kHz USV. While group-housed rats showed the expected preference, i.e., approach, toward 50-kHz USV, the response was even stronger in short-term isolated rats (i.e., 1 day), possibly due to a higher level of social motivation. In contrast, no approach was observed in long-term isolated rats (i.e., 4 weeks). Importantly, deficits in approach were reversed by peer-mediated re-socialization and could not be observed after post-adolescent social isolation, indicating a critical period for social development during adolescence. Together, these results highlight the importance of social experience for affiliative behavior, suggesting a critical involvement of play behavior on socio-affective information processing in rats.

Keywords: affiliative behavior; juvenile social isolation; negative symptoms; rough-and-tumble play; schizophrenia.

Figures

Figure 1
Figure 1
Experimental design of the three studies to assess the impact of post-weaning social isolation on approach behavior induced by pro-social 50-kHz USV. (A) Experimental designs: Experiment 1: Post-weaning Social Isolation—Effects; Experiment 2: Post-weaning Social Isolation—Rescue; and Experiment 3: Post-adolescent Social Isolation—Effects. (B) Schematic illustration of the rat developmental profile, highlighting the rough-and-tumble play period.
Figure 2
Figure 2
Setup of the 50-kHz USV radial maze playback paradigm. (A) Elevated eight arm radial maze equipped with two ultrasonic microphones and two ultrasonic loudspeakers positioned opposite to each other (only one ultrasonic microphone and the active loudspeaker are shown). The rat's behavioral responses during playback of acoustic stimuli were recorded with a video camera positioned above the radial maze. (B) Schematic illustration of the radial maze, depicting area definitions to assess approach behavior, with arms close to the loudspeaker denoted as proximal, central arms as neutral, and opposite arms as distal. (C) Acoustic stimuli were presented by an ultrasonic loudspeaker (sampling rate: 192 kHz; 16 bit), with accurate playback of acoustic stimuli being confirmed by means of ultrasonic microphones. (D) Testing was performed under dim red light.
Figure 3
Figure 3
Post-weaning social isolation induces behavioral inhibition in response to pro-social 50-kHz USV similar to alarm 22-kHz USV and NOISE. (A–C) Exemplary spectrograms of acoustic stimuli used for playback, namely (A) 50-kHz USV, (B) 22-kHz USV, and (C) background noise (NOISE). (A′–C′) Bar graphs depicting changes in locomotor activity as assessed by means of total arm entries per min [entries/min] displayed by rats exposed to 4 weeks of NO ISO (left), SHORT ISO (middle), and LONG ISO (right), post-weaning, in response to (A′) 50-kHz USV, (B′) 22-kHz USV, and (C′) NOISE, in Experiment 1: Post-weaning Social Isolation—Effects. (A″–C″) Pie charts depicting changes in stimulus-directed locomotor activity as assessed by means of numbers of proximal (black), neutral (gray), and distal (white) arm entries displayed as percentages by rats exposed to 4 weeks of NO ISO (left), SHORT ISO (middle), and LONG ISO (right), post-weaning, during the baseline period (5 min; upper row; PRE) and during playback (1 min; lower row; DUR) in response to (A″) 50-kHz USV, (B″) 22-kHz USV, and (C″) NOISE, in Experiment 1: Post-weaning Social Isolation—Effects. The red dashed circles represent 100% of the total number of arm entries during the baseline period (average over all nine experimental groups). The sizes of the circles depicting proximal (black), neutral (gray), and distal (white) arm entries represent total number of arm entries as percentage of 100%. *p < 0.050 compared to LONG ISO; #p < 0.050 compared to baseline locomotor activity.
Figure 4
Figure 4
Post-weaning but not post-adolescent social isolation leads to a lack of approach behavior in response to pro-social 50-kHz USV that can be reversed by re-socialization: within-group comparisons. (A–C) Line graphs depicting changes in side preferences as assessed by the time spent [s/min] on proximal (black) and distal (white) arms displayed by rats exposed to 4 weeks of (A) NO ISO, (B) SHORT ISO, and (C) LONG ISO, post-weaning, during the baseline period (5 min; PRE) and during playback (1 min; DUR) in response to 50-kHz USV in Experiment 1: Post-weaning Social Isolation—Effects. (D–F) Line graphs depicting changes in side preferences as assessed by the time spent [s/min] on proximal (black) and distal (white) arms displayed by rats exposed to 4 weeks of (D) NO ISO, (E) SHORT ISO, and (F) LONG ISO, post-weaning, plus one additional week of peer rearing, during the baseline period (5 min; PRE) and during playback (1 min; DUR) in response to 50-kHz USV in Experiment 2: Post-weaning Social Isolation—Rescue. (G–I) Line graphs depicting changes in side preferences as assessed by the time spent [s/min] on proximal (black) and distal (white) arms displayed by rats exposed to 4 weeks of (G) NO ISO, (H) SHORT ISO, and (I) LONG ISO, post-adolescent, during the baseline period (5 min; PRE) and during playback (1 min; DUR) in response to 50-kHz USV in Experiment 3: Post-adolescent Social Isolation—Effects. *p < 0.050 compared to distal arm time.
Figure 5
Figure 5
Post-weaning but not post-adolescent social isolation leads to a lack of approach behavior in response to pro-social 50-kHz USV that can be reversed by re-socialization: between-group comparisons. (A) Bar graphs depicting changes in side preferences as assessed by the time spent [s/min] on proximal arms during playback in response to 50-kHz USV (1 min) vs. during the baseline period (5 min), displayed by rats exposed to 4 weeks of NO ISO (left), SHORT ISO (middle), and LONG ISO (right), post-weaning, in Experiment 1: Post-weaning Social Isolation—Effects. *p < 0.050 compared to LONG ISO. (B) Bar graphs depicting changes in side preferences as assessed by the time spent [s/min] on proximal arms during playback in response to 50-kHz USV (1 min) vs. during the baseline period (5 min), displayed by rats exposed to 4 weeks of LONG ISO, post-weaning, in Experiment 1: Post-weaning Social Isolation—Effects (left), 4 weeks of LONG ISO, post-weaning, plus one additional week of peer rearing in Experiment 2: Post-weaning Social Isolation—Rescue (middle), 4 weeks of LONG ISO, post-adolescent, in Experiment 3: Post-adolescent Social Isolation—Effects (right). *p < 0.050 compared to EXP 1.

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