The Biological Significance of Acoustic Stimuli Determines Ear
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© 2015. Published by The Company of Biologists Ltd | The Journal of Experimental Biology (2015) 00, 1-8 doi:10.1242/jeb.114694 1 RESEARCH ARTICLE 63 2 64 3 65 4 The biological significance of acoustic stimuli determines ear 66 5 67 6 preference in the music frog 68 7 69 8 Fei Xue1,2, Guangzhan Fang2,*, Ping Yang2, Ermi Zhao1,2, Steven E. Brauth3 and Yezhong Tang2,* 70 9 71 10 72 11 73 12 ABSTRACT prey, predator activities and conspecific behaviors (Rogers et al., 2013; 74 13 Behavioral and neurophysiological studies support the idea that Vallortigara, 2006). 75 Macaca fuscata 14 right ear advantage (REA) exists for perception of conspecific vocal It has been reported that Japanese macaques ( ) 76 15 signals in birds and mammals. Nevertheless, few studies have best discriminate conspecific vocalizations using the right ear 77 16 focused on anuran species that typically communicate through (Petersen et al., 1978). Similarly, mice best discriminate conspecific 78 17 vocalization. The present study examined the direction and ultrasonic communication calls presented to the right ear (Ehret, 79 Macaca mulatta 18 latencies of orientation behaviors in Emei music frogs (Babina 1987). Perhaps for this reason, rhesus monkeys ( ) 80 19 daunchina) produced in response to six auditory stimuli emitted preferentially orient their heads to the right side when conspecific 81 20 by a speaker placed directly behind the subjects. The stimuli calls are presented from a position directly behind the subjects, 82 21 included male advertisement calls produced from within burrow while turning to the left when presented with interspecific sounds 83 22 nests, which have been shown to be highly sexually attractive (Hauser and Andersson, 1994). The same head orientation task has 84 Zalophus californianus 23 (HSA), calls produced from outside burrows, which are of low sexual been conducted on sea lions ( ) (Böye et al., 85 Equus caballus Canis 24 attractiveness (LSA), screech calls produced when frogs are 2005), horses ( ) (Basile et al., 2009) and dogs ( 86 familiaris 25 attacked by snakes, white noise, thunder and silence. For all ) (Reinholz-Trojan et al., 2012; Siniscalchi et al., 2008), 87 26 sound stimuli except the screech, the frogs preferentially turned to yielding results comparable to those obtained with rhesus monkeys. 88 27 the right. Right ear preference was strongest for HSA calls. For the Although REA has been reported in many species using head 89 28 screech and thunder stimuli, there was an increased tendency for orientation preference, such tests have not as yet been carried out in 90 29 subjects to move further from the speaker rather than turning. These anuran species despite the fact that anurans rely strongly on vocal 91 30 results support the idea that in anurans, right ear preference is communication. Right limb preferences in predator avoidance, body 92 31 associated with perception of positive or neutral signals such as the righting and nose scraping have been demonstrated behaviorally in 93 32 conspecific advertisement call and white noise, while a left ear anurans (Bisazza et al., 1996, 1997; Dill, 1977; Lippolis et al., 2002; 94 33 preference is associated with perception of negative signals such Malashichev and Nikitina, 2002; Robins et al., 1998; Robins and 95 34 as predatory attack. Rogers, 2002, 2006; Rogers, 2002), while neural networks in the 96 35 left hemisphere have been shown to play the predominant role in the 97 36 KEY WORDS: Right ear advantage, REA, Auditory perception, production and perception of vocal signals (Bauer, 1993; Fang et al., 98 37 Conspecific calls, Mating strategy, Emotion 2012). Furthermore, left hemisphere dominance for vocalization/ 99 38 auditory perception has been shown to be related to right limb 100 39 INTRODUCTION preference in humans (Knecht et al., 2000; Perlaki et al., 2013), non- 101 40 Lateralization of function for neural structures has been identified in human mammals (Fitch et al., 1993; Güven et al., 2003; Hopkins 102 41 diverse vertebrate species at the individual and population levels and Cantero, 2003; Ρençe, 2002) and birds (Cynx et al., 1992; 103 42 (MacNeilage et al., 2009; Rogers and Andrew, 2002; Vallortigara et al., Ducker et al., 1986), especially for species utilizing vocal signals for 104 43 2011). In mammals, auditory system lateralization has been shown to social communication. Thus, it is reasonable to hypothesize that 105 44 take the form of right ear advantage (REA) such that the organism tends asymmetry for the production and perception of vocal signals is also 106 45 to preferentially process conspecific vocal signals with the right ear related to limb preference in anurans and that lateralization of 107 46 while interspecific and environment sounds are preferentially auditory perception would also be reflected in the behavior of these 108 47 processed using the left ear (Kimura, 2011; Vallortigara and Rogers, species. 109 48 2005). In principle, hemispheric lateralization could improve cognitive In a previous study in the Emei music frog, Babina daunchina 110 49 processing by allowing each hemisphere to specialize, thereby (Chang 1933), we investigated the effects of presentation of various 111 50 avoiding the simultaneous initiation of incompatible responses acoustic stimuli including male advertisement calls on relative 112 51 (Rogers, 2000; Rogers et al., 2004). Accordingly, animals with REA electroencephalogram (EEG) power in the delta, alpha and beta 113 52 could theoretically process acoustic information more efficiently and bands (Fang et al., 2012). Babina males produce advertisement calls 114 53 thus respond more rapidly to environmental signals related to hunting from within hidden burrows whose resonant properties alter the 115 54 acoustic properties of the calls (Chen et al., 2011; Cui et al., 2012, 116 55 1Key laboratory of Bio-resources and Eco-environment, Ministry of Education, 2010). Phonotaxis experiments have shown that 70% of female 117 56 School of life sciences, Sichuan University, Chengdu, Sichuan 610064, People’s Babina prefer calls produced from within the burrows, which are 118 Republic of China. 2Department of Herpetology, Chengdu Institute of Biology, 57 Chinese Academy of Sciences, No.9 Section 4, Renmin South Road, Chengdu, hence more highly sexually attractive (HSA) than those produced 119 58 Sichuan 610041, People’s Republic of China. 3Department of Psychology, from outside the burrows, which are less sexually attractive (LSA) 120 59 University of Maryland, College Park, MD 20742, USA. (Cui et al., 2012) and the male Babina prefer competing vocally 121 60 *Authors for correspondence ([email protected]; [email protected]) with HSA calls rather than with LSA calls (Fang et al., 2014a). 122 61 Electrophysiological studies show that relative power in the alpha, 123 62 Received 28 September 2014; Accepted 27 December 2014 delta and beta bands declines or increases with time in the left but 124 1 RESEARCH ARTICLE The Journal of Experimental Biology (2015) 00, 1-8 doi:10.1242/jeb.114694 125 100 187 List of abbreviations in situ 126 Turn 188 CRH corticotrophin releasing hormone Move away 127 189 EEG electroencephalogram No response 128 HSA high sexual attractiveness 80 190 129 LI laterality index 191 130 LSA low sexual attractiveness 192 131 MA movement angle 60 193 MD movement distance 132 194 REA right ear advantage 133 195 TA turn angle 40 134 WN white noise 196 135 197 136 198 20 137 not right mesencephalon, with the most notable changes occurring Percentage of response pattern 199 138 during playbacks of HSA calls (Fang et al., 2014b). As the anuran 200 139 midbrain receives auditory information derived primarily from the 201 0 140 contralateral auditory nerve (Wilczynski, 1988; Wilczynski and HSA LSA Screech Thunder WN Silence 202 141 Endepols, 2006), our results support the idea that REA is brought 203 142 about by structural asymmetry superimposed with attention Fig 1. The percentage of behavioral response patterns to different stimuli. 204 ‘ ’ 143 modulation (Fang et al., 2014b). However, behavioral evidence is Turn in situ was scored if the frog turned around but moved away from the 205 initial position no more than one snout–tail length. ‘No response’ was scored if 144 required to test the theory that REA occurs in frogs. 206 the frog stayed in the original position without any action until the end of the 145 The present study aimed to examine the behavioral REA trial. ‘Move away’ was scored if the frog moved more than one snout–tail length 207 146 responses of the Emei music frog. As animals habituate to from the initial position. HSA, high sexual attractiveness advertisement call; 208 147 repeated auditory stimulations using a given stimulus, such a LSA, low sexual attractiveness advertisement call; WN, white noise. 209 148 procedure can produce biased results for ear-advantage measures 210 149 (Siniscalchi et al., 2008). Furthermore, it has been shown that the Behavioral response lateralization varied between stimuli 211 150 population level of lateralization reflects the proportion of lateralized Lateralization of turning in situ is shown in Fig. 2. Frogs preferred 212 151 individuals (Ghirlanda and Vallortigara, 2004; Vallortigara, 2006). turning to the right side more than to the left in response to the HSA 213 2 152 Thus, the population level rather than the individual level of call (a single sample Chi-square test: χ2=6.760, P<0.05). Although 214 153 lateralization was measured in the present study. As previous EEG more frogs turned right than left in response to the LSA call, this 215 154 studies have shown that conspecific calls most strongly activate the difference was not significant. The tendency to turn rightwards was 216 155 left hemisphere of animals with REA, we predicted that music frogs greater for HSA than for LSA calls despite the fact that the 217 156 would turn generally rightwards in order to improve discrimination difference was not significant (Fisher’s exact test: P>0.05, two- 218 157 when hearing conspecific calls, with a stronger preference for HSA sided).