Macroscopic characteristics of the praying mantis electroretinogram

Journal of Insect Physiology 59 (2013) 812–823

Contents lists available at SciVerse ScienceDirect

Journal of Insect Physiology journal homepage: www.elsevier.com/locate/jinsphys

Macroscopic characteristics of the praying mantis electroretinogram Barbara Popkiewicz, Frederick R. Prete ⇑ Department of Biology, Northeastern Illinois University, 5500 N. St. Louis Ave., Chicago, IL 60625, USA

a r t i c l e

i n f o

Article history: Received 7 February 2013 Received in revised form 2 May 2013 Accepted 7 May 2013 Available online 16 May 2013 Keywords: Insect visual system Praying mantis Mantodea ERG Electroretinogram

a b s t r a c t We described the macroscopic characteristics of the praying mantis ERG in three species, Tenodera aridifolia sinensis, Sphodromantis lineola, and Popa spurca. In all cases, when elicited by square wave light pulses longer than 400 ms, light adapted (LA) ERGs consisted of four component waveforms: a cornea negative transient and sustained ON, a cornea negative transient OFF, and a cornea positive sustained OFF. The former two ON, and the latter OFF components were attributed to photoreceptor depolarization and repolarization, respectively. Metabolic stress via CO2 induced anoxia selectively eliminated the transient OFF (independent of its effect on the other components) suggesting the transient OFF represents activity of the lamina interneurons on which the photoreceptors synapse. Dark adapted (DA) ERGs differed from LA ERGs in that the sustained ON and OFF amplitudes were larger, and the transient ON and OFF components were absent. Increased stimulus durations increased the amplitudes and derivatives of, and decreased the latencies to the maximum amplitudes of the OFF components. Increasing stimulus intensity increased the amplitude of the sustained ON and OFF components, but not the transient OFF. These results suggest that the mantis’ visual system displays increased contrast coding efficiency with increased light adaptation, and that there are differences in gain between photoreceptor and lamina interneuron responses. Finally, responses to luminance decrements as brief a 1 ms were evident in LA recordings, and were resolved at frequencies up to 60 Hz. Ó 2013 Elsevier Ltd. All rights reserved.

1. Introduction The insect electroretinogram (ERG) is a transcorneal, extracellular recording representing the summed, electrical activity occurring within the distal optic lobe in response to changes in illumination. The resulting complex field potential is understood to represent the activity of the ommatidia retinula (photoreceptor) cells and, in some preparations, the activity of their postsynaptic targets in the first optic neuropil, the lamina monopolar cells (LMCs; e.g., Coombe, 1986; Geng et al., 2002; Hardie and Weckström, 1990; Heisenberg, 1971). Arguably, the most thoroughly characterized ERG is that of the Dipetran flies, a model system that has been comprehensively analyzed from the macroscopic to the molecular level (e.g., Skingsley et al., 1995, and references therein). When elicited by square wave illumination, the typical Dipteran ERG includes, sequentially, a transient, cornea positive ON component representing the hyperpolarization of the LMCs, followed by one or two cornea negative components caused by photoreceptor depolarization, the first with a short and the second with a long rise and decay time (the ‘‘transient’’ and ‘‘sustained’’ ON ⇑ Corresponding author. Tel.: +1 847 209 3515 (primary), +1 773 442 5724 (office); fax: +1 773 442 5730. E-mail addresses: [email protected], [email protected] (F.R. Prete). 0022-1910/$ - see front matter Ó 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.jinsphys.2013.05.002

components, respectively). Stimulus Offset elicits a cornea negative transient OFF component representing the repolarization of the LMCs (e.g., Coombe, 1986; Hardie and Raghu, 2001; Montell, 1999; Stark and Wasserman, 1972). Other insect systems are less thoroughly described, especially at the macroscopic level, and differences are evident between insect species and across experimental protocols. For instance, some insects display monophasic ERGs without obvious photoreceptor and LMC induced transient ON and OFF components, respectively (e.g., Gryllus bimaculatus, Saifullah and Tomioka, 2002; Locusta migratoria, Schmachtenberg and Bicker, 1999). In addition, although it has received less experimental attention, under certain experimental conditions, stimulus Offset can elicit a cornea positive, sustained OFF response representing photoreceptor hyperpolarization (e.g., Schmachtenberg and Bicker, 1999, Fig. 2B); the sustained OFF follows the LMC induced transient OFF should the latter occur (e.g., Heisenberg, 1971; also see, Heimonen et al., 2012). The absence of the transient ON and OFF components in certain experiments can be due to the brevity of the eliciting stimulus, differences in recording procedures, differences in the eye’s degree of light adaptation, and/or differences in resistance regions within the optic lobe itself, rather than differences in optic lobe activity, per se (Colwell and Page, 1989; Kugel, 1977; Yinon, 1971). In Blattodea, sister taxon to the Mantodea, under certain experimental conditions, the ERG can appear monophasic (e.g., Blattella

B. Popkiewicz, F.R. Prete / Journal of Insect Physiology 59 (2013) 812–823

germanica, Chang and Lee, 2001). However, ERGs recorded from the cockroach Leucophaea maderae included both an initial cornea positive ON and a cornea negative, transient OFF separated by a slowly decaying, sustained ON component (Colwell and Page, 1989). The transients were characterized as being ‘‘enhanced’’ when the recordings were done under dim ambient illumination versus in the dark. In addition, a few of the ERGs recorded by Colwell and Page (1989) displayed a robust sustained OFF (e.g., their Fig. 7). Very little is known about the ERG in mantises, and recordings from different locations in the compound eye can differ. For instance, ERGs recorded from the ventral medial compound eye (i.e., fovea) in dark adapted male Tenodera a. sinensis appeared as monophasic, cornea negative sustained ON potentials. However, when recorded from the lateral compound eye, the sustained ON was initially much sharper, and was followed by a cornea positive sustained OFF at stimulus Offset (Liske, 1999). In contrast, ERGs recorded from the frontal compound eye in larval T. sinensis by Walcher and Kral (1994) included a rapid, very robust cornea negative, transient ON, and a sharp, cornea positive OFF separated by a comparatively low amplitude sustained ON. The differences between the ERGs in these two studies are attributable to differences in recording protocols (e.g., in signal filtering). In most cases, insect ERGs are elicited in order to glean information about, for instance, photoreceptor response dynamics, spectral sensitivities, psychophysical thresholds, aspects of phototransduction, or the circadian and/or molecular modulation of photoreceptor activity, and only a few have included mantises (e.g., Chang and Lee, 2001; Fleissner, 1982; Sontag, 1971, and previous references). These various experimental goals are well met by using only brief stimulus durations. However, the resulting ERGs do not always reveal the transient ON and OFF components, may be too short to distinguish the slower components of the photoreceptor activity, and may not include the sustained OFF component. Given the dearth of information on praying mantises, and as part of a larger, on-going research program investigating their object recognition abilities, we were interested in the macroscopic characteristics of the mantis ERG. In particular, we sought to describe the ERG primarily as it is manifested in the light (versus dark) adapted compound eye, including the component OFF potentials which would be associated with luminance decrements caused by the movement of an object in the visual field (e.g., Gonka et al., 1999; Kral and Prete, 2004). To that end, we analyzed the ERGs of three species of mantis in order to describe both the general characteristics of the ERG, and some of the stimulus parameters that affect those characteristics. 2. Materials and methods 2.1. Mantises We tested a total of twenty mantises of three species, Tenodera aridifolia sinensis (n = 4), Sphodromantis lineola (n = 10), and Popa spurca (n = 6). Adult T. a. sinensis were collected in the vicinity of the campus of Northeastern Illinois University (N41° 58.80570 , W087° 43.10880 ). Other species were lab reared from non-inbred stock according to protocols detailed elsewhere (e.g., Prete, 1999). Experiments were conducted on females except where noted. Mantises were kept in individual containers within an enclosure under a 12/12 h light/dark cycle at 30/25 °C, respectively, and fed an average of one live cricket per day. 2.2. Electrophysiology Mantises were anesthetized by brief exposure to CO2 and restrained by gently folding their legs against the prothorax and

813

snuggly wrapping them with plastic film. The abdomen remained unwrapped so as not to interfere with respiratory movements. The wrapped mantis was affixed to an adjustable armature with bands of tape over the plastic film, and the head was stabilized with a collar of sticky wax. Both recording and indifferent electrodes were constructed from TeflonÒ insulated 0.051 mm dia stainless steel wires with the terminal 0.50 mm stripped of insulation. The indifferent electrode was inserted into the head capsule at its dorsal apex, and the active electrode was inserted into the distal posterior lateral compound eye through a small hole made with the tip of a 28 gauge hypodermic needle. After electrode implantation, mantises were allowed P30 min to recover. Recordings were done under dim (45 lux) ambient illumination (light adapted condition, LA), or after an extended period (>30 min) in complete darkness (dark adapted, DA). Data were recorded from individuals over a 48 h period (although preparations were stable for as long as 72 h; Mantes et al., 2012). After recording, mantises were unwrapped and returned to their home cages. The basic experimental procedure was to record and signal average three to five ERGs separated by 15–30 s inter-stimulus intervals (ISIs) from each mantis in response to each treatment level (e.g., each level of stimulus brightness or duration). This constituted one trial. Inter-trial intervals ranged from 15 to 60 s. A signal averaged value from one trial was considered a single data point statistically; overall averages (averages of the signal averaged values ±1 standard error) were calculated across individuals for each treatment level within experiments. The total number of ERGs on which overall results were based (the number of signal averaged ERGs  the number of treatment levels  the number of mantises in the experiment) are indicted in the results. An exception to this general procedure was that used in the experiments in which CO2 was administered. Therein, only single ERGs were recorded at the specified time intervals so as not to blur the temporal effects of the CO2 administration. Recordings were amplified (Differential Amplifier Model 3000, A-M Systems, Sequim, WA 98382-8338 USA; http://www.a-msystems.com/), and stored to disk via an iWorx model 214 Data Recorder and LabScribe2 v2.348 software (iWorx Systems, Inc., Dover NH 03820 USA; http://www.iworx.com). In general, recording gains were set at 100, and high and low pass filters were set at 0.1 Hz and 1 KHz. Subsequent, offline analyses were done with LabScribe2 v2.348. 2.3. Stimuli Optical stimulation was provided by a 5 mm blue LED (peak k = 458 nm) which yielded more robust ERGs than did longer wavelength light. Unless indicated otherwise, the LED was positioned 10 mm in front, and pointed at the center of the implanted compound eye, and was driven by 5 V square wave pulses produced by the stimulator component of the iWorx data recorder. The brightness of the LED was varied by changing its distance from the eye. We calculated the brightness function to be

Wm2 ¼ 3:2016ðlnðdistance to LED in mmÞÞ þ 16:289: The protocol by which computer generated visual stimuli were presented was based on procedures detailed in previously published studies (e.g., Prete et al., 2011; Prete et al., 2013). Mantises viewed the stimuli on a Dell™ flat screen computer monitor (1024  768 pixels; monitor pixel size = 0.75  0.75 degrees of visual angle [°] at the 25 mm viewing distance). Experiments were done in an otherwise dimly lighted room (62 lux). Each stimulus was a black rectangle (3.8 lux at the screen) that moved against a white background (269 lux). One edge length of each rectangle

814

B. Popkiewicz, F.R. Prete / Journal of Insect Physiology 59 (2013) 812–823

subtended 14°, and the other edge length ranged from 9° to 88°. Stimuli were presented in random order and moved back and forth horizontally through visual field center four times at 120 deg/s in each trail (each horizontal excursion = 120°). All ISIs exceeded 30 s.

around two smaller (4.5 mm inside diameter) tubes, one of which to deliver a gentle stream of CO2 (from a tank of compressed gas), and the other air (from an aquarium pump). 2.6. Statistics

2.4. ERG component waveform measurements Four component waveforms could be reliably and repeatedly identified in a typical mantis LA ERG when it was elicited by a light pulse P400 ms. A representative ERG recorded from an S. lineola is shown in Fig. 1. The four major components included a negative going transient ON component (a), a cornea negative, slowly decaying sustained ON component (b), a transient OFF component (c) and a positive going, slowly decaying sustained OFF component (d). Based on pilot data and previously published reports on other arthropods, we analyzed the ERG waveform components using the dependent measures defined in the Fig. 1 legend. These included the ERG Onset latency (e), both the maximum amplitudes (i.e., the maximum absolute value), and the latencies to the maxima of the transient and sustained ON and OFF components, the mean derivatives of the sustained ON (f) and transient OFF components (g, inset), and the maximum derivative of the sustained OFF component (h). All species tested responded similarly in the experiments in which they participated. In certain figures, we have included exemplary ERGs from one or more species chosen either as the clearest graphical representation of a particular result, or to indicate the degree of response similarity between species. 2.5. Anoxia Previous studies have demonstrated that metabolic stress induced by CO2 or N2 administration causes photoreceptor depolarization (e.g., Dimitracos and Tsacopoulos, 1985; Payne, 1981), and selectively and reversibly eliminates the transient OFF response in insect ERGs (e.g., Agam et al., 2000; Colwell and Page, 1989). Here, anoxia was obtained by blowing CO2 over the abdomen of the tethered mantis. Gasses were administered through a 18  97 mm (inside diameter  length) plastic tube that was slipped over the mantis’ abdomen, and affixed to the same armature on which the mantis was held. The rear of the tube was closed

Fig. 1. The four main components of the waveform are the transient and sustained ON (a, b, respectively), and the transient and sustained OFF (c, d, respectively). The measurements used to analyze the ERG are as follows: the maximum amplitudes (i.e., the largest absolute values), and the latencies to the maximum amplitudes of the transient and sustained ON (a, b); the maximum amplitude and latency to the maximum amplitude of the sustained OFF (d); the latency to the ERG Onset (e) defined as the first recorded point at which the voltage decreased by P50%, and continued to decease thereafter; the mean derivative of the sustained ON between its lowest and highest voltages (f); the amplitude of the transient OFF measured between the maximum and minimum voltages (g, inset), the mean derivative between those two points, and the latency to the transient OFF minimum (c); the maximum derivative of the sustained OFF between its transition from the recovery of the transient OFF and its maximum amplitude (h).

All data were checked for normalcy. Nonparametric repeated measures data were analyzed using the Friedman Test (e.g., Friedman, 1940); parametric repeated measures data were analyzed with an ANOVA. Post-hoc and other two-sample comparisons were done with the Wilcoxon Paired-Sample Test (nonparametric), or ttests (parametric data). Post hoc tests were applied conservatively and only to answer specific experimental questions; multiple comparisons were Bonferroni corrected (alpha = 0.05; individual probabilities are reported in the text). Statistics were done in Excel with the appropriate added modules (e.g., http://www.advancedanalyticsllc.com; http://www.excelcurvefitting.com), or in Data DeskÒ (Data Description, inc., Ithaca, NY 14850, USA, http:// www.datadesk.com). Where indicated, data were normalized using the standard convention of expressing the magnitude of individual responses as proportions of the maximum response for a given parameter. In graphs with a large number of data points, error bars are omitted for clarity. 3. Results 3.1. Stimulus duration In the initial set of experiments, baseline data were collected on 12 mantises (T. a. sinensis, n = 4; S. lineola n = 3; P. spurca n = 5). Fig. 2a and b depicts representative average ERGs (n = 5 traces each) recorded under LA and DA conditions, respectively, from a P. spurca in response to 10–2000 ms light pulses (for clarity, intermediate durations included in the subsequent analyses are not pictured). Within animals, response characteristics were consistent across experiments and surprisingly similar between species. In all cases, LA ERGs elicted by light pulses P400 ms consisted of up to four, identifiable, component waveforms: a sharp, negative going transient ON (Fig. 2a, arrow a) preceding a slowly decaying sustained ON, a fast transient OFF (arrow b), and a positive going, slowly decaying sustained OFF (arrow c). Dark adapted ERGs differed from LA ERGs in two key respects (cf., 2a, b). First, their amplitudes were greater. For instance, in a total of 86 ERGs elicited by 1000 ms light pulses, the maximum amplitudes of the DA sustained ON was as much as 134% greater than the LA maxima in P. spurca, and as much as 450–460% greater in S. lineola and T. a. sinensis. Similarly, the DA sustained OFF maxima ranged from 128% to 187% of the LA maxima in P. spurca and S. lineola, to as much as 363% in T. sinensis. Second, there was a substantial diminution or complete absence of the sharp transient ON and OFF components in the DA ERGs (Fig. 2b). Note, however, the partial reemergence of the transient OFF at the termination of the longest (2000 ms) light pulse due to progressing light adaptation caused by the extended stimulus duration (arrow d). In an analysis of a total of 221 LA and 130 DA ERGs, we found that stimulus Onset responses were relatively consistent. Overall, the median latencies to ERG Onset ranged from 8 to 12 ms under both LA and DA conditions. When light adapted, the median latencies to the transient ON ranged from 42 to 68 ms. The latencies to the sustained ON minima were more labile. Overall, they ranged from 137 to 205 ms in LA, and 93 to 140 ms in DA ERGs. However, this difference was not statistically significant. In LA ERGs, as stimulus duration increased, latencies measured from stimulus Offset to both the transient and sustained OFF

B. Popkiewicz, F.R. Prete / Journal of Insect Physiology 59 (2013) 812–823

815

Fig. 2. Average ERGs (n = 5 each) recorded under light (a) and dark (b) adapted conditions from a P. spurca in response to light pulses ranging from 10 to 2000 ms. The overall response patterns were similar between all three species tested. At stimulus durations less than 400 ms, light adapted ERGs were dominated by the transient and sustained ON potentials (arrow a). At longer stimulus durations, the transient and sustained OFF components emerged (arrows b and c). In contrast, dark adapted ERGs were higher in amplitude and did not contain the transient components. However, at stimulus durations P1000 ms, the transient OFF component began to emerge as light adaptation progressed during the extended stimulus duration (arrow d).

maxima decreased significantly (Fig. 3a and b; Fr P 17.143, p 6 0.0125). In addition, both the amplitudes (Fig. 3c and d) and the mean and maximum derivatives of the transient and sustained OFF potentials, respectively, increased (Fig. 3e and f). Similarly, in DA ERGs, the latencies to the sustained OFF maxima decreased, and both the maximum amplitudes and derivatives increased with stimulus duration (data not shown; Fr P 18.89, p 6 0.0123). Put simply, in both light and dark adapted ERGs, the OFF responses occurred sooner, faster, and reached higher amplitudes in response to the termination of progressively longer light pulses. This suggests that like other insects, mantises display improved contrast coding as light adaptation proceeds (which would be the case as stimulus duration increased; e.g., Heimonen, 2008; Juusola et al., 1994; Weckström and Laughlin, 1995). 3.2. Stimulus intensity Fig. 4a and b depicts representative average ERGs (n = 5 traces each) recorded at five representative intensities from one S. lineola and one P. spurca. Normalized average amplitudes of the transient and sustained ON, sustained OFF, and transient OFF potentials (based on a total of 640 ERGs) are plotted against normalized stimulus intensity (V/logI plots) in the subsequent four graphs (Fig. 4c–f). In both species, increased stimulus intensity elicited larger transient and sustained ON, and sustained OFF components (18.30 6 Fr 6 48.61, p < 0.00001). However, the transient OFF was not so affected (asterisks in Fig. 4a, b, and graph f; Fr 6 8.79, p = 0.552). The transient and sustained ON responses in both species were well characterized by similar logistic models. However, the sustained OFF amplitudes displayed a steeper rise over the middle range of stimulus intensities for S. lineola than they did for P. spurca. Similar stimulus intensity dependent differences in the gains between the receptor generated sustained ON and OFF components, and the putative LMC generated transient OFF component have been documented in the ERGs of other insects (e.g., Heisenberg, 1971).

3.3. Anoxia Anoxia induced by CO2 or N2 has been used as a noninvasive, reversible tool to indicate whether the transient OFF reflects the activity of cells distinct from the photoreceptors which generate the sustained ON and OFF components (e.g., Colwell and Page, 1989; Goldsmith, 1960; also see Lantz and Mauro, 1978; Wong et al., 1976). We applied this methodology to seven light adapted mantises (two female and one male S. lineola, and four female P. spurca). The technique had consistent and similar effects in all of the mantises tested. In general, CO2 Onset elicited transient, erratic changes in the ERG which were especially pronounced in P. spurca. These effects sometimes included increases in the voltage noise manifested as seemingly random, spontaneous ‘‘spike like’’ potentials (e.g., Goldsmith, 1960; Payne, 1981). After these initial changes subsided, the ON and sustained OFF amplitudes initially increased (as seen in other insects). Next, the transient OFF disappeared, followed by the diminution and/or disappearance of the transient ON, leaving only the sustained ON and OFF potentials. These effects reversed in a consistent sequence after cessation of CO2 with or without the subsequent administration of air. Specifically, the sustained ON and OFF components returned to baseline levels, and the transient ON reappeared. The transient OFF which was the first to disappear, returned last. This sequence of changes can be seen in the ERGs recorded from a male S. lineola shown in Fig. 5. Both the ON and OFF transients were clearly evident in the baseline ERG (asterisks, Fig. 5a, bottom trace). After 30 s of CO2 administration, the transient and sustained ON amplitudes temporarily increased (the former to 147% of baseline amplitude), and the transient OFF disappeared (arrow a). Thereafter, the transient ON progressively decreased and did not return to baseline amplitude until CO2 was turned off and air was administered for 260 s (arrow b). The transient OFF did not reappear for an additional 180 s (arrow c). After 800 s of air administration, the ERG had returned to its baseline profile (Fig. 5b, top trace). We found the same pattern of effects in the four female S.

816

B. Popkiewicz, F.R. Prete / Journal of Insect Physiology 59 (2013) 812–823

lineola and P. spurca tested. Despite some individual differences in the degree to which the sustained ON and OFF amplitudes fluctuated initially, the transient OFF component was always the most vulnerable to CO2, and was rapidly and selectively eliminated by its administration. Further, the transient OFF did not reappear until all of the other components had become reestablished, sometimes not reaching even 50% of its baseline amplitude for more than 2000 s after the other components had returned to their baseline levels. 3.4. OFF responses The fact that mantises are visually guided predators for whom sequential, luminance decrements (versus increments) are the pivotal stimulus characteristic representing object movement (e.g., Prete et al., 2013) led us to assess the effects of repetitive luminance decrements on the ERG under light adapted conditions. Experimental results based on 225 total ERGs recorded from four P. spurca, three S. lineola, and one T. a. sinensis were similar across species. Representative average ERGs (n = 5 per trace) for two of the species are shown in Fig. 6a–c. When the mantises viewed sequential 500 ms luminance decrements (i.e., LED off) punctuating continuous illumination (LED on), each decrement was followed by a transient OFF with an average latency of 29.00

(±4.85 sd) ms to its initial maximum, and 47.44 (±3.84 sd) ms to its subsequent minimum (right and left facing arrows, respectively in Fig. 6a). We included both latencies in this analysis because the latter will become obscured, as explained below. In each case, the transient OFF was followed by a characteristic sustained OFF (latency = 475.67 ± 28.47 sd ms). However, note that for both mantises, (though more obviously for S. lineola), the termination of the luminance decrement (i.e., the next LED Onset) attenuated the sustained OFF. In addition, each light Onset elicited a characteristic, sharp transient ON with a latency of 39.44 (±2.11 sd) ms (e.g., asterisk in Fig. 6a). When the durations of the luminance decrements were reduced to 100 ms (Fig. 6b), a robust transient OFF was still evident (right facing arrows), and occurred with similar latencies to the maxima and minima (24.67 ± 1.56 sd and 42.83 ± 1.80 sd ms, respectively). However, the sustained OFFs were substantially attenuated by the termination of the luminance decrements (asterisks). Then, after the cessation of each decrement, a transient ON occurred but with significantly shorter latencies than in the previous 500 ms series (21.00 ± 1.04 sd ms; t(paired) = 19.46, p < 0.0001; left facing arrows). When the duration of the luminance decrements was again reduced by a factor of five (to 20 ms), the sustained OFF was all but eliminated (Fig. 6c). However, the transient OFF maxima occurred with the same latencies as seen in the 100 ms series (i.e.,

Fig. 3. Average normalized latencies (a, b), amplitudes (c, d), and derivatives (e, f) associated with the transient and sustained OFF potentials based on a total of 192 light adapted ERGs recorded from three species. In all cases, increased stimulus durations caused significant decreases in latencies, and increases in amplitudes and derivatives of the OFF components. That is, the OFF responses occurred sooner, faster, and reached greater amplitudes in response to the termination of progressively longer light pulses. Similar effects were seen in dark adapted ERGs.

B. Popkiewicz, F.R. Prete / Journal of Insect Physiology 59 (2013) 812–823

817

Fig. 4. (a, b) Average light adapted ERGs (n = 5 traces each) elicited by light pulses varying in intensity from 1.88–11.14 Wm2 (inset). Data in graphs c–f are based on 640 total ERG’s recorded from six mantises. Scatter plots were fitted with the logistic function y ¼ A þ ððB  AÞ=ð1 þ ððC=xÞD ÞÞÞ, wherein y = the normalized avg. amplitude, A and B = the final minimum and maximum y values, respectively, C = the stimulus level at which the middle y value is attained, and D = the slope factor (i.e., the Hill coefficient). As light intensity increased there was a significant increase in the transient and sustained ON (c, d), and the sustained OFF amplitudes (e). However, the transient OFF amplitude was not so affected ((f) asterisks in a, b).

22.00 ± 1.15 sd ms; right facing arrows). Interestingly, this was approximately 2 ms after each LED Onset. At this point, the transient OFF minimum became confounded with the transient ON. However, the distinct, negative going potential following each decrement occurred with a latency comparable to the transient OFF minima in the 100 ms series (i.e., 44.83 ± 1.34 sd ms; asterisks, Fig. 6c). This suggests both that the waveform reflects (at least in part) the transient OFF potential, and that the negative going leg of the potential obscured any ON response that may have occurred after the termination of the brief (20 ms) decrement. Further reductions of the luminance decrement duration did not further change the overall shape of the ERG (Fig. 6d), but did significantly affect the mean latency to the transient OFF maxima and subsequent local minima (Fr P 30.02, p 6 0.0001; Fig. 6e). That is, brighter mean luminance levels (i.e., briefer decrements in this experiment), and consequent increased levels of light adaptation were associated with more rapidly occurring OFF responses (cf., Fig. 3). In addition, reducing the luminance decrements from 20 to 1 ms, significantly reduced the overall amplitudes of the responses (Fr = 36.00, p 6 0.00002; Fig. 6f). The way in which sequential luminance decrements can affect the ERG using more biologically relevant stimuli is seen in Fig. 7a and b. These eight recordings are representatives of 77 total trials

during each of which one of seven rectangular stimuli moved horizontally across the visual field four times (as described in Section 2). The sequential luminance decrements caused by the moving stimuli consistently elicited robust cornea negative deflections as they passed through visual field center irrespective of the orientation of the rectangles (Fig. 7a and b). However, only the larger stimuli (which created the largest decrements) elicited a subsequent, robust sustained OFF response (downward pointing arrows in the four rightmost ERGs). These data are consistent with the previous experimental results in which longer lasting luminance decrements were associated with more robust sustained OFF responses (cf., Fig. 6a–c). Although the overall amplitude of the sustained OFF maxima increased as stimulus size increased (F(1,6) = 142.77, p < 0.0001), the largest increase occurred when the stimuli exceeded 486°2 (arrow, Fig. 7c). Noteworthy is the fact that this is also the size over which these stimuli become poor releasers of appetitive behavior from this species of mantis (e.g., Kral and Prete, 2004, and references therein). We assessed the frequency at which the mantises could resolve sequential luminance decrements such as those in the previous two experiments by presenting five mantises (three S. lineola and two P. spurca) with square wave light pulses separated by equal

818

B. Popkiewicz, F.R. Prete / Journal of Insect Physiology 59 (2013) 812–823

Fig. 5. Effects of CO2 induced anoxia and reversal by air administration on light adapted ERGs recorded from a male S. lineola. The sequence of anoxia induced events was consistent across mantises, species, and experimental protocols. Note the sharp transient ON and OFF components in the baseline ERG (asterisks, bottom trace in panel a). CO2 Onset elicited initial amplitude increases in the sustained ON and OFF components, followed by the disappearance of the transient OFF (arrow a). Thereafter, the transient ON diminished and disappeared (top trace in panel a, 440 s CO2). These effects reversed in a consistent sequence in response to CO2 cessation (panel b): first, the sustained ON and OFF amplitudes returned to baseline levels, followed by the reappearance of the sharp transient ON (arrow b). Finally, the transient OFF reemerged (arrow c).

duration interstimulus intervals (ISIs) such that each total series lasted 1000 ms (e.g., ten 50 ms light pulses separated by 50 ms ISIs). The frequencies tested were 5, 10, 20, 40, 50, 60, 70, 80, 90 and 100 Hz under both LA and DA conditions. The characteristics of the ERG waveforms in this experiment were consistent with other data reported here, including the fact that the components differed between the LA and DA conditions. For instance, average ERGs (n = 3 traces each) recorded from an S. lineola in response to 100 ms stimulus/ISI durations are shown in Fig. 8a. In the LA ERG (upper trace), the 100 ms ISI was long enough to allow for the occurrence of a sustained OFF potential that peaked 112.50 (±1.00 sd) ms after the termination of each light pulse (arrow 3). In turn, each of the sustained OFFs obscured the subsequent ON components (arrow 1). Hence, under LA conditions, the local maxima of the oscillations were the peak amplitudes of the sustained OFFs (arrows 3, a, upper trace). The local minima were created by the transient OFFs which occurred with latencies of 38.80 (±1.179 sd) ms after each light pulse Offset (arrows 2, b, upper trace). In this ERG, the terminal sustained OFF occurring at the end of the stimulus series (arrow 4, upper trace) peaked at 314 ms after stimulus Offset indicating that the four preceding sustained OFFs reached their maxima approximately 12.50 ms after the Onset of, and were attenuated by each subsequent light pulse. In contrast, the DA ERG (Fig. 8a, lower trace) was dominated by the sustained ON and OFF components which created the local maxima and minima defining its oscillations (arrows a, b). These occurred with latencies of 103.6 (±0.894 sd) and 116.5 (±5.0 sd) ms, respectively. The terminal sustained OFF (arrow 4, lower trace) reached its maximum amplitude 790 ms after the final stimulus Offset. Again, this indicated that the preceding OFF potentials were attenuated by each subsequent light pulse. There are two other noteworthy points in these data. First, unlike the LA responses, the periodic, overall oscillations in the DA recordings were carried on a slower, positive going voltage change that represented the gradual, continuing light adaptation caused by the repetitive light

pulses. Second, as light adaptation progressed, both transient ON and OFF potentials began to appear within the larger sustained potential oscillations (arrows 1, 2, lower trace, respectively). Reductions in the ERG oscillations due to the decreasing stimulus/ISI durations (i.e., increasing frequency) were calculated as the change in average amplitudes between the largest, adjacent, local minima and maxima (as indicated, e.g., by arrows a and b in Fig. 8a) during the middle 500 ms of each 1000 ms trial. Measurements were collected over this interval to avoid the initial and terminal ON and OFF responses, respectively. We found no species differences so data were pooled. The average oscillation amplitudes collected from a total of 470 ERGs normalized within LA and DA conditions are plotted against the log of the stimulus frequency in Fig. 8b (note that most of the error bars are hidden by the symbols). Under both LA and DA conditions, increasing frequency had a significant, depressing effect on the oscillation amplitudes (Fr P 33.53, p 6 0.00003). Curves fitted to the data predict an amplitude reduction to 20% of its maximum (dashed line) at frequencies over 60 and 40 Hz, respectively. These values were consistent with the observed frequencies at which the overall oscillations fell out of synchrony with the stimuli. These transition points are marked with asterisks in Fig. 8c and d. These graphs depict average ERGs (n = 3 traces each) recorded from an S. lineola in response to a continuous 1000 ms light pulse (bottom traces) and seven representative stimulus/ISI frequencies under LA and DA conditions (panels c and d, respectively). Recordings from P. spurca were virtually identical.

4. Discussion The experiments reported here represent an initial description of the praying mantis electroretinogram as it appears in T. a. sinensis, S. lineola, and P. spurca. The latter two genera, Sphodromantis and Popa are both from Africa; the former, Tenodera is originally

B. Popkiewicz, F.R. Prete / Journal of Insect Physiology 59 (2013) 812–823

819

Fig. 6. (a–c) Representative ERGs in response to sequential luminance decrements punctuating continuous LED illumination in P. spurca and S. lineola (top and bottom traces, respectively). Decrements lasting P100 ms (a, b) elicited clear transient On (asterisk in a, labeled arrows in b), and transient OFF components (labeled arrows in a, b). The transient OFFs were followed by sustained OFFs that became attenuated when the decrement terminated (e.g., asterisks in b). Luminance decrements lasting 620 ms (c) all but eliminated the sustained OFF. However, a transient OFF persisted (asterisks in c). Further, the latencies to the transient OFF maxima (downward pointing arrows in c) were the same as when the decrements were longer (i.e., 22.00 ± 1.15 sd ms; cf., downward pointing arrows in ac). When decrements lasted 20 ms or less, the transient OFF minima became confounded with the subsequent transient ON. However, the minima (asterisks in c) occurred at latencies consistent with those to the transient OFF minima when the decrements were longer than 20 ms (i.e., 44.83 ± 1.34 sd ms). Further reductions in decrement duration significantly reduced the transient OFF amplitudes (d, f), and the latencies to the transient OFF maxima and the subsequent local minima (e).

an Asian genus. However, Sphodromantis is much more closely related to Tenodera than to Popa. Based on molecular data (Svenson and Whiting, 2009), S. lineola and T. a. sinensis are part of a single, small monophyletic group. Interestingly, Tenodera is the only Asian component in its clade; the remaining taxa are African. Popa spurca is part of a more basal clade containing the African Liturgusinae, Angelinae and Vatinae. Despite the phylogenetic distance between Popa and the other two genera, all of the species displayed fundamental similarities in their ERGs, suggesting a conservation of visual information processing mechanisms at least between these lineages.

4.1. Organization of the mantis compound eye pertinent to the ERG Based on the few species studied, mantises are understood as having apposition type compound eyes (Horridge and Duelli, 1979). As in other insects, each ommatidium contains eight photoreceptors, the six largest of which (R1–R6) contribute to a fused rhabdom along the entire length; the two smaller photoreceptors (R7, R8) contribute only to a portion thereof. In T. sinensis, the R1–R6 axons from each ommatidium synapse on at least three lamina monopolar cells (LMCs) in retinotopically organized units called ‘‘cartridges’’ (Leitinger et al., 1999). Axons from the LMCs, and R7, R8 (which pass through the lamina), contribute to the external optic chiasm and synapse in the medulla, the next more proximal neuropil (Leitinger et al., 1999).

4.2. Photoreceptor mediated ON and OFF responses As in other insects, the cornea negative transient and sustained ON components of the mantis ERG represent photoreceptor depolarization, and, presumably, the sustained OFF component represents their hyperpolarization (Howard et al., 1984; Liske, 1999; Sontag, 1971; Walcher and Kral, 1994). In other insects for which there is data, graded photoreceptor potentials are mediated by the phototransduction induced opening of TRP and TRPL cation channels, and are subsequently shaped by antagonistic voltage sensitive potassium currents (e.g., Agam et al., 2000; Skingsley et al., 1995). However, these mechanisms have not been confirmed in mantises. When elicited by a square wave light pulse lasting at least 400 ms under light adapted conditions, the mantis ERG ON response included a sharp, negative going, rapidly recovering transient component followed by a second, much more slowly decaying waveform, the sustained ON. The latter often included a second, small negative going deflection. These two ON components may represent the differential responses of so-called ‘‘hyperadapting’’ versus ‘‘slow/non-adapting’’ photoreceptors, respectively, that have been well characterized in the cockroach (Heimonen et al., 2012). In contrast, DA ON responses differed both in their overall amplitude, and in the absence of the initial, sharp transient ON. These data are consistent with those reported by Liske (1999) and Walcher and Kral (1994) for T. a. sinensis. The amplitudes and more slowly progressing ON response seen under dark adapted

820

B. Popkiewicz, F.R. Prete / Journal of Insect Physiology 59 (2013) 812–823

c

a

b

Fig. 7. The representative ERGs in panels a and b were recorded from an S. lineola in response to black, rectangular, computer generated stimuli that moved back and forth horizontally through visual field center four times per trial at 120 deg/s (each trace represents one trial). The stimuli included a 1414°2 (leftmost ERGs) and six elongated rectangles measuring 14° by 9–88°. The latter moved parallel or perpendicular to their direction (panel a and b, respectively). Each stimulus excursion elicited robust negative going potentials when it passed through visual field center, the amplitudes of which were not affected by stimulus size. However, the amplitudes of the subsequent sustained OFF components (downward pointing arrows in the rightmost ERGs) increased dramatically as stimuli enlarged (c). The largest stimuli (P486°2) elicited the largest sustained OFF responses and are also poor releasers of appetitive behavior for this species of mantis (arrow in c indicates transition point).

conditions could be a product of mechanisms affecting overall photoreceptor sensitivity, phototransduction speed, or voltage induced rectifying potassium currents. For instance, regional variations in ommatidia morphology, acceptance angles, and sensitivity have been documented in some mantis species (Barros-Pita and Maldonado, 1970; Horridge and Duelli, 1979; Rossel, 1979). In particular, ommatidia acceptance angles in the fovea of the mantis Tenodera australasiae increase from 0.74° when light adapted, to 1.1° when dark adapted during the day, and to 2° when dark adapted at night; increases in the dorsal compound eye acceptance angles are even larger (2.4°, 3.2°, and 6°, respectively; Rossel, 1979). Hence, the sensitivity differences in DA versus LA eyes appear to be affected both by acute responses to changes in ambient illumination, and by endogenous physiological rhythms (e.g., Horridge et al., 1981; Howard et al., 1984; Mantes et al., 2012). However, the underlying mechanisms are yet to be determined in mantises. As sit-and-wait or opportunistic predators, mantises must rely on the unpredictable, intermittent appearance of prey. As a result, they are generally food deprived in the field (Hurd, 1999, pers. comm.), and must be prepared to capture prey at any time, even under dim light conditions (e.g., at dawn or dusk, or when perched amid dense foliage). In addition, many species engage in mate seeking and courtship behavior at night, and some display crepuscular locomotor activity patterns (Mantes et al., 2012; Gemeno et al., 2005; Matsura and Inoue, 1999; Robinson and Robinson, 1979). So, despite being thought of as strictly diurnal, mantises can be ‘‘surprisingly active at night’’ (Horridge et al., 1981; Rossel, 1979). That being the case, one would expect their visual systems to function well under both bright and dim light conditions, and differ anatomically from those of their closest relatives, the Blattodea, whose visual systems are specialized for life in the dark (Heimonen et al., 2006, 2012). One known difference is the greater degree of convergence of photoreceptor axons onto lamina interneurons in the cockroach, P. americana versus the mantis, T. sinensis (Heimonen et al., 2006; Leitinger et al., 1999). These different arrangements confer enhanced visual sensitivity to the cockroach (useful under low light conditions) and increased visual acuity to the mantis (useful for accurate prey recognition). At the termination of light pulses lasting longer than 400 ms, mantis ERGs displayed robust, slowly decaying, cornea positive

potentials (the sustained OFF component), the amplitude and rise times of which varied directly with stimulus intensity and duration. This is a characteristic response to ‘negative contrasts’ (i.e., luminance decrements) by depolarizing photoreceptors (e.g., Heimonen et al., 2012; Laughlin and Weckström, 1993; Matic and Laughlin, 1981). The amplitudes of such sustained OFF responses have been shown to vary directly with both the degree of photoreceptor saturation, and the degree of contrast between a transient luminance decrement and the background brightness. This is consistent with the sustained OFF components’ decreased latencies, increased amplitudes, and shorter rise times caused by increases in stimulus duration, and with the decreases in sustained OFF amplitudes caused by decreases in stimulus intensities seen in the mantis ERGs. 4.3. Transient OFF The reversible, selective elimination of the transient OFF by CO2 induced anoxia suggests that in mantises, this ERG component is a product of cells other than the photoreceptors. In other insects, the transient OFF is understood to represent the repolarization of the lamina monopolar cells (LMCs) on which the photoreceptors synapse (Coombe, 1986; Hardie and Raghu, 2001; Heisenberg, 1971; Montell, 1999; Stark and Wasserman, 1972). Based on its anatomical complexity, Heisenberg (1971) suggested that the lamina may serve as an initial information processing step immediately following photoreception, and this seems to be the case in some insects (e.g., Borst, 2009). His reasoning was based in part on the nonlinear relationship between the ERG sustained ON and transient OFF amplitudes under varying stimulus intensities. A similar relationship was seen here in which diminished stimulus intensity affected the former more than the latter in both S. lineola and P. spurca. Hence, it may be the case that information processing in the mantis lamina is similarly complex, and represents the initial information processing step in object recognition. 4.4. Luminance decrements Ultimately, we are interested in the so-called OFF responses seen in the mantis ERG under light adapted conditions. In the wild,

B. Popkiewicz, F.R. Prete / Journal of Insect Physiology 59 (2013) 812–823

a

b

c

d

821

Fig. 8. (a) Representative average ERGs (n = 3 traces each) elicited by alternating 100 ms light pulses and inter-stimulus intervals (ISIs) under light adapted (LA) and dark adapted (DA) conditions (upper and lower trace, respectively). Arrows 1 and 2 indicate transient ON and OFF components, respectively; arrows 3 and 4 indicate sustained OFF components. In both LA and DA ERGs, the overall oscillation amplitudes were defined by the amplitude differences between adjacent local maxima and minima that occurred during the middle 500 ms of the 1000 ms stimulus presentation (e.g., arrows a, b in each ERG). In the DA ERG (lower) trace, the transient ON and OFF (arrows 1 and 2) begin to appear as light adaptation progresses due to the additive effects of the light pulses. Graph b depicts the normalized average ERG oscillation amplitude versus stimulus frequency from 5 to 125 Hz. Data were fitted with the function y = (A + (B/(1 + exp((((1)*C) + (D*ln(x))) + (E*x))))) where y = the normalized avg. amplitude, A = minimum y value, B = range of y values, C and E = the x value when the middle y value is attained, and D = the slope factor. Under both light and dark adapted conditions, increasing stimulus/ISI frequency significantly decreased oscillation amplitudes. Amplitudes dropped to 20% of their maximum values at stimulus frequencies above 40 and 60 Hz under DA and LA conditions, respectively. Above these frequencies, ERG oscillations fell out of synchrony with the stimulus frequencies. Panels c and d are characteristic ERGs recorded from an S. lineola in response to a continuous 1000 ms light pulse (bottom traces), and seven representative stimulus/ISI frequencies. Asterisks indicate transition points at which ERG oscillations fell out of synchrony with the stimuli. Recordings from S. lineola and P. spurca were indistinguishable.

object movement is manifested as a series of luminance decrements moving across the retinae (e.g., Gonka et al., 1999; Kral, 2012; Kral and Prete, 2004; Prete et al., 2011, 2013). So, for instance, under the experimental conditions reported here, we found that a large, moving luminance decrement such as might be caused by a predator, elicits both a robust transient OFF and a subsequent sustained OFF response. In contrast, however, very brief sequential decrements such as might be caused by a small, fast moving prey item, elicit a transient but not a sustained OFF. The important point for our research is that if the transient OFF represents the activity of lamina monopolar cells in mantises, and lamina activity represents an initial information processing step (rather than just a relay mechanism), then lamina activity plays a nontrivial role in the ini-

tial stages of the sensory-motor transforms that link visual input to target directed appetitive behaviors. However, confirmation of this working hypothesis requires considerable additional research. The ability to resolve sequential luminance decrements at frequencies from 40 to 60 Hz under our experimental conditions is sufficient to resolve the movement of the prey items on which mantises are known to feed in the wild (e.g., Hurd, 1999), or the movements of peering induced retinal image displacement (e.g., Kral, 2012). However, we do recognize that flicker resolution varies with a number of factors including light intensity and object-tobackground contrast ratios. Consequently, the maximum resolvable flicker frequencies are likely to be higher under daylight conditions in the field than in the lab. However, the data reported

822

B. Popkiewicz, F.R. Prete / Journal of Insect Physiology 59 (2013) 812–823

here are consistent with results of analogous experiments characterizing mantises and some other slow moving insects as having so-called ‘‘slow’’ (versus ‘‘fast’’) eyes (e.g., Miall, 1978; Weckström and Laughlin, 1995). That said, little is known about mantis ecology outside of a few temperate zone species, and many live among dense foliage, hang under leaves, and catch prey at dusk when light levels are low. Hence, the relationship between the remarkable visual systems for which mantises are known and their ecological niches remains largely unexplored with just a few notable exceptions (e.g., Kral, 2012). This initial analysis of the macroscopic characteristics of the mantis ERG opens the door to a number of experimental questions regarding its details. However, the limited data on mantis ecology makes it difficult to draw parallels with other insects. For instance, it would be especially instructive to explore the relationships between phototransduction mechanisms and ecologically meaningful behaviors in mantises as has been done in the case of mate recognition by drone honey bees (Vallet and Coles, 1993). Given their robust visual abilities and unique behaviors, the praying mantises are a potentially valuable model system for such analyses. Acknowledgements We thank the Department of Biology and the NEIU Student Center for Science Engagement (SCSE), an initiative of the U.S. Department of Education (CCRAA HSIP031C080027), and the Collaboration and Retention through Environmental and Agricultural Research (CREAR) program for their support. In particular, we acknowledge the collegial support that we received from Dr. Marcelo Sztainberg, Dr. Nancy Wrinkle, Dr. Stephanie Levi, and Marilyn Saavedra-Leyva. We are also indebted to the other members of our research team for their collegial and enthusiastic help in various aspects of this ongoing project: Edgar Mantes, Andrew Uridailes, Wil Bogue, and Benjamin Prete. We thank the journal editors and anonymous referees for their thoughtful comments and suggestions, Dr. Aaron Schirmer (Department of Biology, NEIU), Dr. Karl Kral (Institute of Zoology, Karl-Franzens-Universität, Graz), and Arlene Bonnet for comments on earlier versions of this manuscript, and Frank Wieland for his advice on mantis phylogeny. In all cases, the experimental animals were treated with the appropriate concerns and we operated in accordance with all applicable ethical and animal care guidelines. This work was supported in part by an SCSE Summer Research Opportunities Grant and a CREAR grant to FRP. References Agam, K., von Campenhausen, M., Levy, S., Ben-Ami, H.C., Cook, B., Kirschfeld, K., Minke, B., 2000. Metabolic stress reversibly activates the Drosophila lightsensitive channels TRP and TRPL in vivo. The Journal of Neuroscience 20, 5748– 5755. Barros-Pita, J.C., Maldonado, H., 1970. A Fovea in the praying Mantis Eye lI. Some morphological characteristics. Zeitschrift für vergleichende Physiologie 67, 79– 92. Borst, A., 2009. Drosophila’s view on insect vision. Current Biology 19, R36–R47. http://dx.doi.org/10.1016/j.cub.2008.11.001. Chang, H.-W., Lee, H.-J., 2001. Inconsistency in the expression of locomotor and ERG circadian rhythms in the German cockroach, Blattella germanica (L.). Archives of Insect Biochemistry and Physiology 48, 155–166. Colwell, C.S., Page, T.L., 1989. The electroretinogram of the cockroach Leucophaea maderae. Comparative Biochemistry and Physiology A 92, 117–123. Coombe, P.E., 1986. The large monopolar cells L1 and L2 are responsible for ERG transients in Drosophila. Journal of Comparative Physiology A 159, 655–665. Dimitracos, S.A., Tsacopoulos, M., 1985. The recovery from a transient inhibition of the oxidative metabolism of the photoreceptors of the drone (Apis mlifera). Journal of Experimental Biology 119, 165–181. Fleissner, G., 1982. Isolation of an insect circadian clock. Journal of Comparative Physiology A 149, 311–316. Friedman, M., 1940. A comparison of alternative tests of significance for the problem of m rankings. The Annals of Mathematical Statistics 11, 86–92.

Gemeno, C., Claramunt, J., Dasca, J., 2005. Nocturnal calling behavior in mantids. Journal of Insect Behavior 18, 389–403. Geng, C., Leung, H.T., Skingsley, D.R., Iovchev, M.I., Yin, Z., Semenov, E.P., Burg, M.G., Hardie, R.C., Pak, W.L., 2002. The target of Drosophila photoreceptor synaptic transmission is a histamine-gated chloride channel encoded by ort (hclA). Journal of Biological Chemistry 277, 42113–42120. Goldsmith, T.H., 1960. The nature of the retinal action potential, and the spectral sensitivities of ultraviolet and green receptor systems of the compound eye of the worker honeybee. Journal of General Physiology 43, 775–799. Gonka, M.D., Laurie, T.J., Prete, F.R., 1999. Responses of movement-sensitive visual interneurons to prey-like stimuli in the praying mantis Sphodromantis lineola (Burmeister). Brain Behavior and Evolution 54, 243–262. Hardie, R.C., Raghu, P., 2001. Visual transduction in Drosophila. Nature 413, 186– 193. Hardie, R.C., Weckström, M., 1990. Three classes of potassium channels in large monopolar cells of the blowfly Calliphora vicina. Journal of Comparative Physiology A 167, 723–736. Heimonen, K., 2008. Processing of visual information in dim light. Functional variability, matched filtering and spike coding in cockroach (Periplaneta americana) photoreceptors. Dissertation, the University of Oulu. ISBN 978951-42-8949-1. Heimonen, K., Salmela, I., Kontiokari, P., Weckström, M., 2006. Large functional variability in cockroach photoreceptors: optimization to low light levels. The Journal of Neuroscience 26, 13454–13462. Heimonen, K., Immonen, E.-V., Frolov, R.V., Salmela, I., Juusola, M., Vähäsöyrinki, M., Weckström, M., 2012. Signal coding in cockroach photoreceptors is tuned to dim environments. Journal of Neurophysiology 108, 2641–2652. Heisenberg, M., 1971. Separation of receptor and lamina potentials in the electroretinogram of normal and mutant Drosophila. Journal of Experimental Biology 55, 85–100. Horridge, G.A., Duelli, P., 1979. Anatomy of the regional differences in the eye of the mantis ciulfina. Journal of Experimental Biology 80, 165–190. Horridge, G.A., Duniec, J., Marcelja, L., 1981. A 24-hour cycle in single locust and mantis photoreceptors. Journal of Experimental Biology 91, 307–322. Howard, J., Dubs, A., Payne, R., 1984. The dynamics of phototransduction in insects. Journal of Comparative Physiology A 154, 707–718. Hurd, L.E., 1999. Ecology of praying mantises. In: Prete, F.R., Wells, H., Wells, P.H., Hurd, L.E. (Eds.), The Praying Mantises. The Johns Hopkins University Press, Baltimore, MD, USA, pp. 43–46. Juusola, M., Kouvalainen, E., Järvilehto, M., Weckström, M., 1994. Contrast gain, signal-to-noise ratio, and linearity in light-adapted blowfly photoreceptors. Journal of General Physiology 104, 593–621. Kral, K., 2012. The functional significance of mantis peering behavior. European Journal of Entomology 109, 295–301. Kral, K., Prete, F.R., 2004. In the mind of a hunter: the visual world of the praying mantis. In: Prete, F.R. (Ed.), Complex Worlds from Simpler Nervous Systems. MIT, Cambridge, MA, pp. 75–115. Kugel, M., 1977. The time course of the electroretinogram of compound eyes in insects and its dependence on special recording conditions. Journal of Experimental Biology 71, 1–6. Lantz, R.C., Mauro, A., 1978. Alteration of sensitivity and time scale in invertebrate photoreceptors exposed to anoxia, dinitrophenol, and carbon dioxide. The Journal of General Physiology 72, 219–231. Laughlin, S.B., Weckström, M., 1993. Fast and slow photoreceptors—a comparative study of the functional diversity of coding and conductances in the Diptera. Journal of Comparative Physiology A 172, 593–609. Leitinger, G., Pabst, M.A., Kral, K., 1999. Serotonin-immunoreactive neurones in the visual system of the praying mantis: an immunohistochemical, confocal laser scanning and electron microscopic study. Brain Research 823, 11–23. Liske, E., 1999. The hierarchical organization of mantid behavior. In: Prete, F.R., Wells, H., Wells, P.H., Hurd, L.E. (Eds.). The Johns Hopkins University Press, Baltimore, MD, USA, pp. 224–250. Mantes, E.S., Bogue, W., Popkiewicz, B.W., Urdiales, A.F., Prete, F.R., Schirmer, A.E., 2012. Circadian, behavioral, and physiological rhythms in the praying mantis, Hierodula multispina (Insecta: Mantodea). In: Proceedings of the Northeastern Illinois University Third Annual Faculty Research and Creative Activities Symposium, Nov 16, 2012, Chicago, IL, p. 4. Matic, T., Laughlin, S.B., 1981. Changes in the intensity-response function of an insect’s photoreceptors due to light adaptation. Journal of Comparative Physiology A 145, 169–177. Matsura, T., Inoue, T., 1999. The ecology and foraging strategy of Tenodera augustipennis. In: Prete, F.R., Wells, H., Wells, P.H., Hurd, L.E. (Eds.), The Praying Mantises. Macmillan, New York, pp. 61–68. Miall, R.C., 1978. The flicker fusion frequencies of six laboratory insects, and the response of the compound eye to mains fluorescent ‘ripple’. Physiological Entomology 3, 99–106. Montell, C., 1999. Visual transduction in Drosophila. Annual Review of Cell and Developmental Biology 15, 231–268. Payne, R., 1981. Suppression of noise in a photoreceptor by oxidative metabolism. Journal of Comparative Physiology A 142, 181–188. Prete, F.R., 1999. Rearing techniques, developmental time, and life span data for labreared Sphodromantis lineola. In: Prete, F.R., Wells, H., Wells, P.H., Hurd, L.E. (Eds.), The Praying Mantises. The Johns Hopkins University Press, Baltimore, MD, pp. 303–310.

B. Popkiewicz, F.R. Prete / Journal of Insect Physiology 59 (2013) 812–823 Prete, F.R., Komito, J.L., Domínguez, S., Svenson, G., López, Y.L., Guillen, A., Bogdanivich, N., 2011. Prey recognition in three morphologically distinct species of praying mantis. Journal of Comparative Physiology A 197, 877–894. Prete, F.R., Dominguez, S., Komito, J.L., Theis, R., Dominguez, J.M., Hurd, L.E., Svenson, G.J., 2013. Differences in appetitive responses to computer-generated visual stimuli by female Rhombodera basalis, Deroplatys lobata, Hierodula membranacea, and Miomantis sp. (Insecta: Mantodea). Journal of Insect Behavior 26, 261–282. Robinson, M.H., Robinson, B., 1979. By dawn’s early light: matutinal mating and sex attractants in a neotropical mantid. Science 205, 825–827. Rossel, S., 1979. Regional differences in photoreceptor performance in the eye of the praying mantis. Journal of Comparative Physiology A 13l, 95–112. Saifullah, A.S.M., Tomioka, K., 2002. Serotonin sets the day state in the neurons that control coupling between the optic lobe circadian pacemakers in the cricket Gryllus bimaculatus. The Journal of Experimental Biology 205, 1305– 1314. Schmachtenberg, O., Bicker, G., 1999. Nitric oxide and cyclic GMP modulate photoreceptor cell responses in the visual system of the locust. The Journal of Experimental Biology 202, 13–20.

823

Skingsley, D.R., Laughlin, S.B., Hardie, R.C., 1995. Properties of histamine-activated chloride channels in the large monopolar cells of the dipteran compound eye: a comparative study. Journal of Comparative Physiology A 176, 611–623. Sontag, C., 1971. Spectral sensitivity studies on visual system of praying mantis, Tenodera sinensis. Journal of General Physiology 57, 93–112. Stark, W.S., Wasserman, G.S., 1972. Transient and receptor potentials in the electroretinogram of Drosophila. Vision Research 12, 1771–1775. Svenson, G.J., Whiting, M.F., 2009. Reconstructing the origins of praying mantises (Dictyoptera, Mantodea): the roles of Gondwanan vicariance and morphological convergence. Cladistics 25, 468–514. Vallet, A.M., Coles, J.A., 1993. The perception of small objects by the drone honeybee. Journal of Comparative Physiology A 172, 183–188. Walcher, F., Kral, K., 1994. Visual deprivation and distance estimation in the praying mantis larva. Physiological Entomology 19, 230–240. Weckström, M., Laughlin, S.B., 1995. Visual ecology and voltage-gated ion channels in insect photoreceptors. Trends in Neurosciences 18, 17–21. Wong, F., Wu, C.F., Mauro, A., Pak, W.L., 1976. Persistence of the prolonged light induced conductance change in arthropod photoreceptors on recovery from anoxia. Nature, London 264, 661–664. Yinon, U., 1971. The visual mechanisms of Tenebrio molitor: changes in the electroretinogram as function of the stimulus duration. Journal of Experimental Biology 54, 737–744.