A Stereologic Analysis of Mustached Bat Auditory Cortex
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Brain Research 1045 (2005) 164 – 174 www.elsevier.com/locate/brainres Research report Is humanlike cytoarchitectural asymmetry present in another species with complex social vocalization? A stereologic analysis of mustached bat auditory cortex Chet C. Sherwooda,b,*, Mary Ann Raghantia,b, Jeffrey J. Wenstrupc aDepartment of Anthropology, Kent State University, 226 Lowry Hall, Box 5190, Kent, OH 44242-0001, USA bSchool of Biomedical Sciences, Kent State University, Kent, OH 44242-0001, USA cDepartment of Neurobiology, Northeastern Ohio Universities College of Medicine, Rootstown, OH 44272, USA Accepted 15 March 2005 Available online 19 April 2005 Abstract Considerable evidence suggests that left hemispheric lateralization for language comprehension in humans is associated with cortical microstructural asymmetries. However, despite the fact that left hemispheric dominance for the analysis of species-specific social vocalizations has been reported in several other species, little is known concerning microstructural asymmetries in auditory cortex of nonhumans. To test whether such neuroanatomical lateralization characterizes another species with complex social vocalizations, we performed stereologic analyses of Nissl-stained cells in layer III of area DSCF in mustached bats (Pteronotus parnellii). Area DSCF was selected because it contains neurons which are sensitive to several temporal features of conspecific vocalizations. Primary visual cortex (V1) was also studied as a comparative reference. We measured neuron densities, glial densities, and neuronal volumes in both hemispheres of 10 adult male bats. Results indicate that these variables are not significantly lateralized in area DSCF or V1. Additionally, magnopyramidal cells (i.e., the largest 10% of neurons from both hemispheres) were not asymmetric in their frequency of distribution at the population level. Although several individual bats had asymmetric neuron distributions, consistent hemispheric bias was not evident. Absence of population- level microstructural asymmetry in area DSCF of mustached bats suggests alternative evolutionary scenarios including: (1) microstructural lateralization of auditory cortical circuitry may be a unique adaptation for human language, and (2) the specialized biosonar function of mustached bat auditory cortex may require symmetrical cytoarchitectural structure. Resolution of these alternatives will require further data on the microstructure of auditory cortex in species with lateralized perception of acoustic social communication. D 2005 Elsevier B.V. All rights reserved. Theme: Neural basis of behavior Topic: Neuroethology Keywords: Asymmetry; Mustached bat; Social vocalization; Stereology; DSCF; V1 1. Introduction majority of individuals, regions of the left cerebral hemi- sphere are specialized for the comprehension and production Neuroanatomical and behavioral lateralization are wide- of language [17,57]. Left hemispheric dominance for the spread across vertebrate species [47]. The link between perception and analysis of species-specific social voca- behavioral lateralization and neocortical asymmetry is lizations, however, is not unique to humans and has perhaps best established in humans where, in the vast been reported in several nonhuman species, especially among Old World monkeys. Evidence from behavior, experimental lesion studies, and functional imaging, for * Corresponding author. Fax: +1 330 672 2999. instance, indicates that macaques display a left hemisphere E-mail address: [email protected] (C.C. Sherwood). bias for discriminating acoustic features of species-specific 0006-8993/$ - see front matter D 2005 Elsevier B.V. All rights reserved. doi:10.1016/j.brainres.2005.03.023 C.C. Sherwood et al. / Brain Research 1045 (2005) 164–174 165 vocal calls [20,21,41,42,44]. In addition, house mouse To address the lack of data concerning microstructural mothers exhibit a right ear preference in their orientation asymmetries in nonhumans, the current study examines response to the ultrasonic distress calls of their pups [8]. whether cortical asymmetries occur in an echolocating bat. Finally, chick and starling individuals express unilateral The greater mustached bat, Pteronotus parnellii,isan dominance in their perception of conspecific vocal calls, insectivorous species of the neotropics that displays two however, they do not exhibit strong population-wide direc- highly developed audio–vocal behaviors. In echolocation, it tional bias to the left [15,35]. Taken together, these findings emits a multiharmonic sonar signal and analyzes the suggest that lateralized auditory processing of communica- resulting echoes to navigate and to catch flying insects. In tion signals is common across vertebrates, possibly due to social communication, it uses a complex repertoire of the constraint of reducing temporal delays associated with vocalizations, with well-defined rules for combining simple interhemispheric transfer in the analysis of complex, time- syllables into composites that can last a second or more [32]. dependent, serial streams of acoustic information as Mustached bats are highly social, often forming groups of represented by many species-specific vocal calls [46]. tens of thousands in which adults of both sexes live together In this context, numerous studies have documented for a part of the year but then segregate when females give microstructural asymmetries of auditory cortical areas in birth and nurse their pups [3,18,52]. Since these bats live in humans that putatively relate to perceptual lateralization. A large dark caves, they depend on acoustic communication principal focus of these investigations has been area Tpt (the for many of their social interactions. posterior portion of Brodmann’s area 22), a eulaminate cortex The auditory cortex of this animal displays highly at the core of Wernicke’s area, a polymodal association specialized response properties both to the echoes of sonar region important for language comprehension in humans [1]. signals [40,55] and to social vocalizations [9,39].For In an early study, left hemispheric dominance in the size of example, auditory cortical neurons show sensitivity to area Tpt was demonstrated in four human brain specimens several temporal features of social vocalizations, such as [11]. More recently, long-range intrinsic connections within temporal ordering and timing of syllables, analogous to area Tpt labeled in postmortem brains with lipophilic dyes temporal features that underlie syntax in human speech and revealed greater spacing between interconnected patches in other primate vocal communication systems [9]. Preliminary the left hemisphere compared to the right [12]. The layer III studies of mustached bat auditory cortex suggest that pyramidal cell population also exhibits left hemisphere functional asymmetries occur. In the Doppler-shifted con- dominant asymmetry within several different cortical areas stant frequency area (area DSCF) of primary auditory along the temporal auditory processing stream. For instance, cortex, neurons on the left side appear to respond better to in many auditory areas, including primary auditory cortex communication sounds than to sonar pulse–echo combina- and area Tpt, the left hemisphere has a greater number of the tions, while this was not the case for neurons on the right largest pyramidal cells in layer III, known as magnopyrami- side [30,31]. dal cells, that give rise to long corticocortical association We examined whether cytoarchitectural asymmetries projections [27]. Furthermore, acetylcholinesterase-rich pyr- similar to those reported for area Tpt in humans are present amidal cells display greater cell soma volumes in the left in the auditory cortex of mustached bats. We hypothesized hemisphere of secondary and language-associated areas that asymmetries would be present in area DSCF favoring despite lacking asymmetry in terms of number [28]. Lastly, the left hemisphere. For comparison, we also analyzed left area Tpt has a greater amount of neuropil and contains asymmetries in primary visual cortex (V1), under the axons with thicker myelin sheaths, possibly to facilitate hypothesis that lateralization would not be present, espe- specialized processing of signals with rapid temporal cially considering the extreme visual reduction of this variation, such as speech [2]. species. To test these predictions, we used design-based Unfortunately, there is a paucity of data on the presence stereologic techniques to characterize cellular densities and of analogous microstructural asymmetries in the auditory neuronal volume distributions in layer III and made cortex of nonhuman species. In the only study to directly comparisons between homotopic cortical areas. compare cytoarchitectural asymmetries in layer III of area Tpt in humans and other species, humans were found to have wider minicolumns and greater neuropil space on the 2. Materials and methods left, whereas such asymmetries were absent in chimpanzees and rhesus macaques [5]. Other data, however, indicate the 2.1. Subjects and sample preparation presence of asymmetries in volume [14] and the distribution of inhibitory microcircuitry in area Tpt of macaques [33]. The brains of ten adult male greater mustached bats Overall, these results support the idea that cortical asym- were used in this study. Greater mustached bats (P. parnellii metries comprise an important anatomical substrate for parnellii) were captured in Jamaica, West Indies. In lateralized auditory processing of language in humans