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Tactile Foveation in the Star-Nosed Mole

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Tactile Foveation in the Star-Nosed Mole Original Paper Brain Behav Evol 2004;63:1–12 Received: May 28, 2003 Returned for revision: July 11, 2003 DOI: 10.1159/000073755 Accepted after revision: July 24, 2003 Tactile Foveation in the Star-Nosed Mole Kenneth C. Catania Fiona E. Remple Department of Biological Sciences, Vanderbilt University, Nashville, Tenn., USA Key Words and both distributions were closely correlated with the Somatosensory W Mechanosensory W Saccade W Touch W degree of cortical magnification of the appendage repre- Cortex W Mammals W Star-nosed mole sentations in primary somatosensory cortex (S1). Copyright © 2004 S. Karger AG, Basel Abstract Star-nosed moles have a specialized somatosensory sys- Introduction tem with 22 mechanosensory appendages surrounding the nostrils. A pair of appendages (the 11th pair on the Many mammals with well-developed visual systems ventral midline) acts as the tactile fovea and is used for have a retinal fovea characterized by a high density of detailed investigations. Here we used a high speed video photoreceptors and correspondingly enlarged areas of the camera to document movements of the star while moles central nervous system for processing information from searched for small prey items. Mole foraging behavior this important area of central vision. In humans it has was very fast; the star, which is just over a centimeter in been estimated that only one ten-thousandth of the visual diameter, was touched to different areas of the environ- field is seen with full clarity [see Carpenter, 1988 for ment approximately 13 times per second. This suggests review] and therefore the eyes must be constantly shifted that a mole foraging without interruption could potential- in a saccadic, or jerky, manner in order to analyze a visual ly investigate 46,000 cm2 of surface area per hour. In 100% scene. Some echolocating bats have developed an analo- of 526 trials in which prey was identified and eaten, star- gous organization for their auditory system complete with nosed moles made rapid, saccadic movements of the star an acoustic version of a saccade. For example mustached to investigate the contacted prey with the foveal appen- bats (Pteronotus parnellii) have an acoustic fovea corre- dages. The movements of the star were similar to visual sponding to the 2nd harmonic of their echolocation pulses saccades in other species. Maximum velocity of the star [Suga and Jen, 1976; Suga, 1989] but echos returning during saccades was approximately 40 cm/s, and most from flying prey are often Doppler shifted to a frequency saccades were between 30 and 60 ms in duration. As in outside of the fovea’s narrow range. By constantly shifting the primate visual system, small corrective saccades were the frequency of their outgoing pulses (a behavior called often needed to accurately foveate. We quantified the Doppler shift compensation) bats can focus returning number of contacts different appendages made with prey echos on their acoustic fovea [Schnitzler, 1968] much like items of various sizes during each encounter and com- an eye movement centers important visual information pared this distribution to a previously proposed simula- on the retinal fovea. tion of star movements during prey encounters. The The more recent discovery of a mechanosensory fovea behavior pattern and the simulation produced similar dis- in the star-nosed mole [Catania and Kaas, 1997] provides tributions of contact between the appendages and prey, further evidence for a remarkable degree of convergence © 2004 S. Karger AG, Basel Kenneth C. Catania, PhD ABC Vanderbilt University, Department of Biological Sciences Fax + 41 61 306 12 34 VU Station B 351634 E-Mail [email protected] Accessible online at: Nashville, TN 37235 (USA) www.karger.com www.karger.com/bbe Tel. +1 615 343 1079, Fax +1 615 343 0336, E-Mail [email protected] Downloaded by: Weizmann Inst. of Science 149.126.78.33 - 1/26/2016 10:32:20 PM in the design of sensory systems that handle large volumes A of complex information. Visual, auditory, and somatosen- sory specialists have all hit upon the same solution of div- iding the sensory system into a small, high resolution area for detailed analysis and a larger, low resolution area for scanning a sensory scene. An obvious advantage of this design is the conservation of processing territory in the central nervous system – a large proportion of which is devoted to the representation of the fovea. Although primate eye movements and the behavior of echolocating bats have been the subjects of numerous B C 1 cm investigations [eyes – Carpenter, 1988; Goldberg et al., Nose 2 Cortex 1990; Gaymard and Pierrot-Deseilligny, 1999; Schall and 3 1 Thompson, 1999; bats – Asanuma et al., 1983; Kujirai S1 Nose and Suga, 1983; Simmons, 1989; Suga, 1989], far less is 4 known about tactile foveation in the star-nosed mole. The star consists of 11 pairs of bilaterally symmetric appen- 5 dages surrounding each nostril (numbered 1–11 from the 6 9 8 7 6 5 dorsal most appendage). The tactile fovea is the pair of 7 11 10 4 3 2 relatively small, 11th appendages just above the mouth 10 11 (fig. 1). Here we have documented the movements of the 8 9 1 Fovea star during foraging behavior in the laboratory using a 2 mm 1mm S1 Nose high-speed camera. Our main goal was to provide a Representation description of the star movements in response to tactile stimuli (prey items) of various sizes to assess the proposed Fig. 1. The star-nosed mole and its sensory specializations. A A star- analogy (in the behavioral dimension) between the star- nosed mole emerges from its underground tunnel system showing the 22 appendages that ring the nostrils and the large clawed forelimbs nosed mole’s somatosensory fovea and the visual and used for digging tunnels. B Schematic of the star with the numbering auditory foveas described for other species. We also test system for the separate mechanosensory appendages. The 11th the predictions of a previously proposed simulation, or appendage acts as the tactile fovea. C The primary somatosensory model, of tactile foveation in the star-nosed mole [Catania cortex of the star-nosed mole contains a series of 11 stripes visible in and Kaas, 1997]. This simulation predicts the distribu- cytochrome oxidase processed tissue. These stripes are the areas where information from each tactile appendage is processed [see tion of contacts between the appendages and prey items of Catania and Kaas, 1995]. The anatomical reflection of each appen- different sizes that are encountered during foraging bouts. dage in the cortical map allows the area of each appendage represen- Finally, we revisit the organization of somatosensory cor- tation to be accurately measured and compared to star-nosed mole tex in star-nosed moles in relation to observed behavior behavior (see text). patterns. Materials and Methods worm 1–6 mm in diameter) were placed. A high speed video camera (S-Series MotionScope, Redlake Imaging Corporation) was posi- For our behavioral recordings, four star-nosed moles were tioned below the glass plate and illumination was provided from trapped under PA scientific collecting permit number COL00087. below with two fiber-optic light sources. Behavior was generally The moles were housed separately in 38 ! 55 cm containers filled to filmed at a sampling rate of 250 or 500 frames per second and a a depth of 20 cm with moist peat moss. These home cages were con- shutter speed of 1/2,500 s. Data frames were stored digitally in a vid- nected by a 5 cm diameter plastic tube to a 26 ! 40 cm container eo buffer and then transferred to S-VHS videotape for archiving and filled with 6 cm of water. Fresh water was provided daily. The mole’s scoring. Digital images from high speed video were captured for fig- captive diet consisted mainly of commercially raised nightcrawlers ures from the VHS tapes using a Macintosh G4 computer and iMovie supplemented occasionally with small crayfish. Plastic tubes (5cm2.0 software (Apple Computer). All procedures conformed to Nation- inside diameter) connected the containers to a variety of Plexiglas al Institutes of Health standards concerning the use and welfare of chambers in which the behavioral observations and filming took experimental animals and were approved by the Vanderbilt Univer- place (fig. 2). The bottom floor of the Plexiglas container was a sity Animal Care and Use Committee. removable glass plate on which small prey items (pieces of an earth- 2 Brain Behav Evol 2004;63:1–12 Catania/Remple Downloaded by: Weizmann Inst. of Science 149.126.78.33 - 1/26/2016 10:32:20 PM Results basic pattern of search behaviors and the frequency of tac- tile foveation. The contact of different appendages to prey We filmed trials from the 4 moles as they encountered items was also quantified in 526 behavior trials for com- and ingested prey items (small segments of an earthworm) parison with previous measures of cortical magnification ranging in size from 1.0 to 6.0 mm. Our first goal in this in star-nosed moles [Catania and Kaas, 1997]. study was to examine nose movements to determine the Search Behavior Foraging behavior depends on the star, which is in con- stant motion as these moles explore their underground Prey habitat in search of food. Prey items in the field consist of a variety of small invertebrates found in the wetland hab- Entrance Item itat [Hamilton, 1931]. In the laboratory, we used small pieces of earthworms as prey items in order to document Filming Chamber the movements of the star during foraging. When explor- ing their enclosures and searching for food, moles made a series of high speed touches with the star (13 per second) to different areas of their environment.
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