Elsevier

Brain Research

Volume 1045, Issues 1–2, 31 May 2005, Pages 164-174
Brain Research

Research report
Is humanlike cytoarchitectural asymmetry present in another species with complex social vocalization? A stereologic analysis of mustached bat auditory cortex

https://doi.org/10.1016/j.brainres.2005.03.023Get rights and content

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.

Introduction

Neuroanatomical and behavioral lateralization are widespread across vertebrate species [47]. The link between behavioral lateralization and neocortical asymmetry is perhaps best established in humans where, in the vast majority of individuals, regions of the left cerebral hemisphere are specialized for the comprehension and production of language [17], [57]. Left hemispheric dominance for the perception and analysis of species-specific social vocalizations, however, is not unique to humans and has been reported in several nonhuman species, especially among Old World monkeys. Evidence from behavior, experimental lesion studies, and functional imaging, for instance, indicates that macaques display a left hemisphere bias for discriminating acoustic features of species-specific vocal calls [20], [21], [41], [42], [44]. In addition, house mouse mothers exhibit a right ear preference in their orientation response to the ultrasonic distress calls of their pups [8]. Finally, chick and starling individuals express unilateral dominance in their perception of conspecific vocal calls, however, they do not exhibit strong population-wide directional bias to the left [15], [35]. Taken together, these findings suggest that lateralized auditory processing of communication signals is common across vertebrates, possibly due to the constraint of reducing temporal delays associated with interhemispheric transfer in the analysis of complex, time-dependent, serial streams of acoustic information as represented by many species-specific vocal calls [46].

In this context, numerous studies have documented microstructural asymmetries of auditory cortical areas in humans that putatively relate to perceptual lateralization. A principal focus of these investigations has been area Tpt (the posterior portion of Brodmann's area 22), a eulaminate cortex at the core of Wernicke's area, a polymodal association region important for language comprehension in humans [1]. In an early study, left hemispheric dominance in the size of area Tpt was demonstrated in four human brain specimens [11]. More recently, long-range intrinsic connections within area Tpt labeled in postmortem brains with lipophilic dyes revealed greater spacing between interconnected patches in the left hemisphere compared to the right [12]. The layer III pyramidal cell population also exhibits left hemisphere dominant asymmetry within several different cortical areas along the temporal auditory processing stream. For instance, in many auditory areas, including primary auditory cortex and area Tpt, the left hemisphere has a greater number of the largest pyramidal cells in layer III, known as magnopyramidal cells, that give rise to long corticocortical association projections [27]. Furthermore, acetylcholinesterase-rich pyramidal cells display greater cell soma volumes in the left hemisphere of secondary and language-associated areas despite lacking asymmetry in terms of number [28]. Lastly, left area Tpt has a greater amount of neuropil and contains axons with thicker myelin sheaths, possibly to facilitate specialized processing of signals with rapid temporal variation, such as speech [2].

Unfortunately, there is a paucity of data on the presence of analogous microstructural asymmetries in the auditory cortex of nonhuman species. In the only study to directly 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 left, whereas such asymmetries were absent in chimpanzees and rhesus macaques [5]. Other data, however, indicate the presence of asymmetries in volume [14] and the distribution of inhibitory microcircuitry in area Tpt of macaques [33]. Overall, these results support the idea that cortical asymmetries comprise an important anatomical substrate for lateralized auditory processing of language in humans and may, to some extent, serve a homologous function in other species.

To address the lack of data concerning microstructural asymmetries in nonhumans, the current study examines whether cortical asymmetries occur in an echolocating bat. The greater mustached bat, Pteronotus parnellii, is an insectivorous species of the neotropics that displays two highly developed audio–vocal behaviors. In echolocation, it emits a multiharmonic sonar signal and analyzes the resulting echoes to navigate and to catch flying insects. In social communication, it uses a complex repertoire of vocalizations, with well-defined rules for combining simple syllables into composites that can last a second or more [32]. Mustached bats are highly social, often forming groups of tens of thousands in which adults of both sexes live together for a part of the year but then segregate when females give birth and nurse their pups [3], [18], [52]. Since these bats live in large dark caves, they depend on acoustic communication for many of their social interactions.

The auditory cortex of this animal displays highly specialized response properties both to the echoes of sonar signals [40], [55] and to social vocalizations [9], [39]. For example, auditory cortical neurons show sensitivity to several temporal features of social vocalizations, such as temporal ordering and timing of syllables, analogous to temporal features that underlie syntax in human speech and other primate vocal communication systems [9]. Preliminary studies of mustached bat auditory cortex suggest that functional asymmetries occur. In the Doppler-shifted constant frequency area (area DSCF) of primary auditory cortex, neurons on the left side appear to respond better to communication sounds than to sonar pulse–echo combinations, while this was not the case for neurons on the right side [30], [31].

We examined whether cytoarchitectural asymmetries similar to those reported for area Tpt in humans are present in the auditory cortex of mustached bats. We hypothesized that asymmetries would be present in area DSCF favoring the left hemisphere. For comparison, we also analyzed asymmetries in primary visual cortex (V1), under the hypothesis that lateralization would not be present, especially considering the extreme visual reduction of this species. To test these predictions, we used design-based stereologic techniques to characterize cellular densities and neuronal volume distributions in layer III and made comparisons between homotopic cortical areas.

Section snippets

Subjects and sample preparation

The brains of ten adult male greater mustached bats were used in this study. Greater mustached bats (P. parnellii parnellii) were captured in Jamaica, West Indies. In captivity, male and female bats were housed communally in a large room (8.5′ × 15′ × 8.5′) with incomplete partitions to allow the formation of social groups. The room was heated (78 °F) and humidified (>75% relative humidity) to suit neotropical bats. All procedures on the animals were approved by the Institutional Animal Care

Cell densities and glial–neuron ratios

Table 1 shows cell densities and Table 2 shows glial–neuron ratios from both hemispheres. Glial–neuron ratios were calculated to reflect a possible correlate of metabolic and supportive requirements for greater neuronal activity. Increased glial–neuron ratios, for instance, are associated with environmental enrichment in rats [7]. Asymmetry coefficients were calculated from the data for each individual, and one sample t tests were performed to evaluate whether significant deviations from

Discussion

Our findings demonstrate that interhemispheric asymmetry of layer III cytoarchitectural organization is not present in area DSCF or V1 of male mustached bats. In particular, we did not find population-level asymmetries of neuron density, glial density, glial–neuron ratio, or mean neuron volume. Although several individuals had neuron volume distributions that deviated from symmetry in areas DSCF and V1, there was interindividual variation in the direction of hemispheric bias. Importantly,

Acknowledgments

We thank Carol Grose for providing expert technical assistance. This work was supported by the Wenner-Gren Foundation for Anthropological Research, Kent State University, and research grant R01 DC 00937 from the National Institute on Deafness and Other Communication Disorders.

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