In my post dated Sep. 30, 2009, I briefly discussed the discovery of echolocation as a means for bats to navigate their environment in total darkness and identify insects to feast on. I noted that in echolocating bats a large part of the auditory system is devoted to the processing of ultrasound, that is frequencies higher than the human audible (>20 kHz). A disproportionate number of auditory nerve cells are tuned to analyze the frequencies of the echos of the echolocation calls bats emit. I worked on research with echolocating bats in Gerhard Neuweiler's laboratory at the Institute of Zoology of the Johann Wolfgang Goethe University, Frankfurt am Main. I helped show that exposing a bat to its echolocation frequency activated prominent regions in its auditory midbrain structure known as inferior colliculus (Melzer, 1985). The proclivity in the bat auditory system for a narrow band of ultrasound used for echolocation is known as high frequency filter or acoustic fovea (Neuweiler and others, 1980).
As informative contrast to the bats' fovea for extremely high pitch, a mammal was sought with a fovea for extremely low pitch. It was hoped that a similar association between behaviorally relevant sound and its representation in the brain might exist in species whose hearing is particularly sensitive to infrasound, that is at frequencies beneath the human audible (<20 Hz). Elephants (Herbst and others, 2012) and humpbacked whales are known to produce and hear infrasound, but were considered difficult to study.
By contrast, burrowing rodents were thought to constitute suitable candidates, because they spend much of the day underground and were observed to be able to use seismic vibrations to identify and locate conspecifics and predators. Particularly, gerbils were of interest. They are essentially crepuscular, that is most active above ground at dawn and dusk. They live in semi-arid deserts where compacted gravel and sand carry low frequency sound long distances. Gerbils use hind foot drumming as means of communication. The drumming exhibits species-specific differences and has been observed to alert companions to one's own presence in as much as to approaching predators (Randall, 1997). Differences in the signature of the sound may permit the animals to distinguish between various types of predator, e.g. snakes or birds. Moreover, the sounds may convey to predators that they have been discovered (Randall, 2001).
Christian Winter recruited Jürgen Möller as a junior faculty member to investigate whether gerbils may represent the small mammals with an acoustic fovea for infrasound. He had extensive experience in acoustics, micro-electrode recordings of electrical nerve cell discharges, and animal behavior.
|courtesy J. Möller|
The photograph depicts a sand rat (Psammomys obesus) in the Negev desert at dusk. Sand rats were the largest gerbils in Jürgen's collection. Power density spectra of their drumming's acoustic frequency components were recorded to examine whether the drumming produced infrasound. Broad spectrum audiograms were constructed from recordings of small voltage changes in the inner ear (cochlear microphonics) and from nerve cell activity in the auditory midbrain (inferior colliculus) to investigate whether the animals could hear infrasound.
The results were presented at a joint symposium of Hebrew University of Jerusalem, Université de Lyon, and Johann Wolfgang von Goethe University entitled "Neurobiology and Strategies of Adaptation". The symposium was convened in Frankfurt am Main in 1981. The two figures below show representative results of the frequencies of the sound produced by drumming (A) and of the sound processed by the auditory system (B). The green band covers the frequency range between 0.5 and 1.0 kHz in which the audiograms (B) show peculiar low frequency sensitivity.
|The frequency of the drumming's acoustic components [kHz] (y-axis) is plotted versus time [ms] (x-axis; courtesy J. Möller).|
|The sound pressure level [dB SPL] of the most sensitive response (y-axis) is plotted versus sound frequency [kHz] (x-axis). Cochlear microphonics: CM; nerve cell responses in the inferior colliculus: IC (courtesy J. Möller).|
My project's aim was to visualize pitch-related nerve cell activation in the brain with a functional imaging method (Melzer, 1984). M. Müller (now private docent at the J.W. Goethe University) helped me substantially in this endeavor. The project would not have been possible without the use of the whole-body cryotome in H.-M. Kellner's division at the Hoechst AG's Radiochemical Laboratory.
Animals were exposed to sound of low, medium and high pitch. Pitch is represented tonotopically on the transverse plane through the inferior colliculus. That is, nerve cells in the upward (dorsal) aspect of the structure are particularly sensitive to low frequency sound and become progressively more sensitive to higher frequencies with increasing depth. Functional imaging would reveal the isofrequency domains, permitting us to assess the prominence of low frequency processing in the auditory system.
The figure below shows frequency-related nerve cell activation in transverse slices through the inferior colliculus. Nerve cell activation is coded in pseudo colors (blue: low; red: high). The narrow blue/purple lines near the top are the animals' scalp, that is dorsal is up. The brainstem is at the bottom, that is ventral is down. The animals' left side is on the right.
The progression of bands of elevated nerve cell activation from top to bottom with increasing frequency of stimulation is consistent with the notion of a tonotopic map where frequencies are represented in logarithmic progression. Intriguingly, the low part of the sound spectrum was slightly disproportionally represented. However, such disproportionality is not uncommon and has been observed in a number of species (N. Suga, personal communication).
The narrow bands of activation observed with the middle stimulus frequency conformed most distinctly with a representation of frequencies in discrete isofrequency layers. According to the cochlear microphonics, the animals' ear is most sensitive at this frequency. By contrast, the wide-spread activation at the low frequency and the additional foci at the top of the inferior colliculus at the low and the high frequency did not precisely adhere to the principle of discrete frequency representation. We did not know how to interpret these results.
In hindsight, we were perhaps too narrowly focused on auditory responses. Parts of the inferior colliculus are known to receive somatic sensory input. Sand rats have long mystacial whiskers that are in frequent contact with the soil. Cytoarchitectonic structures known as barrels represent the mystacial whiskers topographically in a large swath of the gerbil's cerebral somatic sensory cortex (Rice and others, 1985). Distinct septa separate the barrels. Nerve cells in the septa are known to be particularly attuned to the processing of stimulus frequency (Melzer and others, 2006). Recent observations show that whiskers may resonate (Moore, 2004) to low frequency vibrations, touch receptors in the whisker follicles transduce frequencies up to 1.0 kHz and possibly greater (Gottschaldt and Vahle-Hinz, 1981), and nerve cells in the somatic sensory pathway may process this information (Kleinfeld and others, 2006). Perhaps, gerbils do possess an infrasound fovea after all! Only the processing of this sound may not be strictly auditory.
- Watching gerbils around the time of an earthquake may prove insightful. A tiny whiskered burrowing rodent, the Northern Pocket Gopher Thomomys talpoides, survived the catastrophic eruption of Mt. St. Helens in 1980 (11/06/09).
- Caldwell and others (2010) produced an impressive demonstration of the importance of vibrations in vertebrate sensation and behavior. The research feature on National Public Radio's Talk of the Nation (Science Friday) yesterday with the title "Rumble in The Jungle" shows red-eyed treefrogs (Agalychnis callidryas) from the rain forests of central America communicating with vibrations mediated by the twig they sit on. Listen to the podcast of Ira Flatow's conversation with Flora Lichtman entitled "Red-Eyed Treefrogs Rumble in the Jungle". The authors of the study, affiliated with Boston University, contributed excellent footage of the frogs' interactions (05/22/10).
- On Apr. 8, 2011, National Public Radio's Talk of the Nation/Science Friday broadcast an insightful segment with the title "Seeing The World Through Whiskers" on the research of Mitra Hartman and her colleagues (Towal and others, 2011) examining whisking in rats with high-speed video (04/11/2011):
- The magnitude 5.8 earthquake on the East Coast on Aug. 23, 2011, centered near Mineral, Virginia, was felt roughly 120 miles away by animals of the National Zoo in Washington D.C., in some instances tens of minutes before humans did. Listen to Ira Flatow's interview with Brandie Smith, Senior Curator of the National Zoological Park, Smithsonian Institution, Washington D.C., entitled "Did you feel it?" on National Public Radio's Talk of the Nation/Science Friday broadcast today (08/26/2011).
- Listen to Dr. Tecumseh Fitch explaining to Audie Cornish of National Public Radio's All Things Considered in his interview with the title "Study: Humans, Elephants User Similar Vocalizations" broadcast today how elephants produce and may use infrasound (08/09/2012).
- Caldwell MS, Johnston GR, McDaniel JG, Warkentin KM (2010) Vibrational signaling in the agonistic interactions of red-eyed treefrogs. Current Biol: doi:10.1016/j.cub.2010.03.069
- Gottschaldt KM, Vahle-Hinz (1981) Merkel cell receptors: structure and transducer function. Science 214:183-186.
- Herbst CT, Stoeger AS, Frey R, Lohscheller J, Titze IR, Gumpenberger M, Fitch WT (2012) How low can you go? Physical production mechanism of elephant infrasonic vocalizations. Science 337: 595-599.
- Kleinfeld D, Ahissar E, Diamond ME (2006) Active sensation: insights from the rodent vibrissa sensorimotor system. Curr Opin Neurobiol 16:435-444.
- Melzer P (1985) A deoxyglucose study on auditory responses in the bat Rhinolophus rouxi. Brain Res Bull 15:677-681.
- Melzer P (1984) The central auditory pathway of the gerbil Psammomys obesus: a deoxyglucose study. Hear Res 15:187-195.
- Melzer P, Sachdev RN, Jenkinson N, Ebner FF (2006) Stimulus frequency processing in awake rat barrel cortex. J Neurosci 26:12198-12205.
- Moore CI (2004) Frequency-dependent processing in the vibrissa sensory system. J Neurophysiol 91:2390-2399.
- Neuweiler G, Bruns V, Schuller G (1980) Ears adapted for the detection of motion, or how echolocating bats have exploited the capacities of the mammalian auditory system. J Acoust Soc Am 68:741-753.
- Randall JA(2001) Evolution and function of drumming as communication in mammals. Am Zoologist 41:1143-1156.
- Randall JA (1997) Species-specific footdrumming in kangaroo rats: Dipodomys ingens, D. deserti, D. spectabilis. Anim Behav 54:1167-1175.
- Rice FL, Gomez C, Barstow C, Burnet A, Sands P (1985) A comparative analysis of the development of the primary somatosensory cortex: interspecies similarities during barrel and laminar development. J Comp Neurol 236:477-495.
- Towal RB, Quist BW, Gopal V, Solomon JH, Hartmann MJZ (2011) The Morphology of the Rat Vibrissal Array: A Model for Quantifying Spatiotemporal Patterns of Whisker-Object Contact. PLoS Comput Biol 7: e1001120. doi:10.1371/journal.pcbi.1001120.
- The text of this post is available for download in pdf-format from the scribd store.
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