Processing of behaviorally relevant temporal parameters of acoustic stimuli by single neurons in the superior olivary nucleus of the leopard frog

Summary Response characteristics of 130 single neurons in the superior olivary nucleus of the northern leopard frog (Rana pipiens pipiens) were examined to determine their selectivity to various behaviorally relevant temporal parameters [rise-fall time, duration, and amplitude modulation (AM) rate of acoustic signals. Response functions were constructed with respect to each of these variables. Neurons with different temporal firing patterns such as tonic, phasic or phasic-burst firing patterns, participated in time domain analysis in specific manners. Phasic neurons manifested preferences for signals with short rise-fall times, thus possessing low-pass response functions with respect to this stimulus parameter; conversely, tonic and phasic-burst units were non-selective and possessed all-pass response functions. A distinction between temporal firing patterns was also observed for duration coding. Whereas phasic units showed no change in the mean spike count with a change in stimulus duration (i.e., all-pass duration response functions), tonic and phasic-burst units gave higher mean spike counts with an increase in stimulus duration (i.e., primary-like high-pass response functions). Phasic units manifested greater response selectivity for AM rate than did tonic or phasic-burst units, and many phasic units were tuned to a narrow range of modulation rates (i.e., band-pass). The results suggest that SON neurons play an important role in the processing of complex acoustic patterns; they perform extensive computations on AM rate as well as other temporal parameters of complex sounds. Moreover, the response selectivities for rise-fall time, duration, and AM rate could often be shown to contribute to the differential responses to complex synthetic and natural sounds.Abbreviations SON superior olivary nucleus - DMN dorsal medullary nucleus - TS torus semicircularis - FTC frequency threshold curve - BF best excitatory frequency - PAM pulsatile amplitude modulation - SAM sinusoidal amplitude modulation - SQAM square-wave amplitude modulation - MTF modulation transfer function - PSTH peri-stimulus time histogram     

The integration of antagonistic reflexes revealed by laser ablation of identified neurons determines habituation kinetics of the Caenorhabditis elegans tap withdrawal response

Previously, we described the circuitry that underlies the tap withdrawal response of the nematode Caenorhabditis elegans. In response to a light mechanosensory stimulus a worm will withdraw, usually by initiating backward locomotion, but occasionally with increased forward locomotion. The form of an animal's response is a product of the balance between two antagonistic reflexes: backward locomotion (reversals) triggered by anterior mechanosensory input and forward locomotion (accelerations) triggered by posterior mechanosensory input. During habituation of this reflex, the frequency of forward and backward locomotion in response to tap is modulated by both experience and interstimulus interval; reversals are more frequent early in a habituation series and at longer Inter stimulus intervals. Single-cell laser microsurgery was used to study each of the subcomponents of the intact behavior during habituation training. Groups of intact or laserablated worms were habituated at either a 10-s or a 60-s inter stimulus interval and the kinetics of habituation in each group was analyzed. We demonstrate that each component of the behavior habituates and does so with kinetics that are consistent with the decrement observed in the intact animal.Abbreviations ALM anterior lateral microtubule - AVM anterior ventral microtubule - ISI interstimuls interval - NGM nematode growth medium - PLM posterior lateral microtubule - PVC posterior ventral interneuron C     

Two types of plasticity in the tentacle withdrawal reflex of Helix aspersa are dissociated by tissue location and response measure

The tentacle withdrawal reflex of the terrestrial snail Helix aspersa was studied in vitro. The reflex is evoked by mechanical stimulation of the nose. Lesion experiments showed that 45% to 75% of the response amplitude is attributable to peripheral pathways alone. The central contribution increases with increasing stimulus intensity.Repeated stimulation produced pure habituation at low stimulus strengths, and habituation mixed with intrinsic sensitization (warm-up effect) at high stimulus strengths. The simultaneous occurrence of habituation and sensitization is consistent with the dual process theory of plasticity. Additional results differentiate the two processes. Habituation can occur without the CNS, whereas intrinsic sensitization requires the CNS. Also, the two processes are differentially effective in their influences on response amplitude and duration: habituation is more effective in determining response amplitude, while sensitization is more effective in determining response duration.Although the establishment of sensitization requires the CNS, 81% of the memory for intrinsic sensitization was localized to the periphery, by lesion experiments. Extrinsic sensitization, caused by stimulation of the medial lip nerve, had similar behavioural effects and a similar memory locus. Both types of sensitization appear to be caused by neuromuscular facilitation mediated by a central pathway.Abbreviations CNS central nervous system - PNS peripheral nervous system - S-R stimulus-response - TRM tentacle retractor muscle     

Gap detection in the starling (Sturnus vulgaris)

Summary Gap-detection thresholds of single units were determined from auditory forebrain neurons of the awake starling. Nine different response types were statistically defined from the discharge pattern to a 400 ms broadband noise stimulus. The gap stimuli consisted of two broadband noise bursts which were separated by a gap ranging from 0.4 to 204.8 ms duration. The median minimumdetectable gap for 121 out of 145 units that had a significant threshold 204.8ms was 12.8 ms; 20% of the neurons showed thresholds between 0.4 and 3.2 ms. The neurons of the nine response types differed significantly in their minimum-detectable gaps; neurons with phasic-tonic and phasic excitation exhibited the best (i.e. shortest) minimum-detectable gaps. The neurons of the three different recording areas (field L, NCM and HV) were significantly different in their minimumdetectable gaps; field L neurons showed the best temporal resolution for gaps in broadband noise. Gap-detection thresholds are compared with psychophysical thresholds determined with the same stimuli and the relevance of forebrain units for temporal resolution is discussed.Abbreviations CS control stimulus - HV hyperstriatum ventrale - HVc hyperstriatum ventrale pars caudalis - NB noise burst - NCM neostriatum caudale pars medialis - NS noise stimulus - SGS standard gap series - TW time window     

Encoding of acoustic directional information by saccular afferents of the sleeper goby, Dormitator latifrons

This paper reports on directional response properties of saccular afferents of the sleeper goby, Dormitator latifrons, to 100-Hz acoustic particle motions with a focus on testing the hypothesis that the response directionality of a fish's auditory afferents derives from the morphological polarity of sensory hair cells in the otolithic organs. Spontaneous rates (SR) and best sensitivities (BS) of saccular afferents ranged from 0 to 162 spikes/sec and from 0.2- to 100-nm RMS displacement. SR did not vary with BS. Most saccular afferents were phase-locked to sinusoidal stimulation and had sustained temporal response patterns with some adaptation. All saccular afferents were directionally sensitive to the stimulus, and the sharpness of directional response curves was determined by a directionality index (DI). The DI ranged from 0.64 to 1.50 (mean=1.02, SE=0.02, n=100) and gradually decreased with stimulus level throughout afferents' response dynamic range. Many afferents had approximately symmetric directional response curves relative to their best response axes (BRA). BRA of most afferents remained constant with stimulus level. The BRA distribution had a peak along an axis that correlates closely with the morphological polarity of saccular hair cells. Therefore, our results strongly support the hypothesis. Accepted: 19 December 1997     

Characterisation of columnar neurons and visual signal processing in the medulla of the locust optic lobe by system identification techniques

We describe visual responses of seventeen physiological classes of columnar neuron from the retina, lamina and medulla of the locust (Locusta migratoria) optic lobe. Many of these neurons were anatomically identified by neurobiotin injection. Characterisation of neuronal responses was made by moving and flash stimuli, and by two system identification techniques: 1. The first-order spatiotemporal kernel was estimated from response to a spatiotemporal white-noise stimulus; 2. A set of kernels to second order was derived by the maximal-length shift register (M-sequence) technique, describing the system response to a two-channel centre-surround stimulus. Most cells have small receptive fields, usually with a centre diameter of about 1.5°, which is similar to that of a single receptor in the compound eye. Linear response components show varying spatial and temporal tuning, although lateral inhibition is generally fairly weak. Second-order nonlinearities often have a simple form consistent with a static nonlinear transformation of the input from the large monopolar cells of the lamina followed by further linear filtering.Abbreviations LMC large monopolar cell - LVF long visual fibre - RF receptive field - SMC small monopolar cell - SVF short visual fibre     

Regulation of melatonin production by light,darkness, and temperature in the trout pineal

Summary The pineal gland of the rainbow trout, Salmo gairdneri, when kept under in vitro perifusion culture conditions, displays a consistently elevated level of melatonin production in darkness (Gern and Greenhouse 1988). Upon light exposure melatonin production falls and stabilizes at a new lower level that is dependent upon the irradiance of the stimulus. To achieve the maximal response for each irradiance, the duration of the stimulus must exceed 30 min. The response amplitude is maximally sensitive to photons presented over durations of 30–45 min; is very insensitive to shorter light exposures; and is maintained with no evidence of adaptation over longer exposures. Temperature plays a role in regulation of melatonin production both in darkness and during light exposure; increased temperature increases melatonin production in darkness and also increases the sensitivity of the response to light. The action spectrum for the response is best fit by the Dartnall nomogram for a vitamin A₁ based rhodopsin with peak sensitivity near 500 nm. The possible adaptive significance of control of melatonin synthesis by light and temperature is considered.Abbreviations LD lightdark cycle - RIA radioimmunoassay - I ¹²⁵ Iodine - HIOMT hydroxyindole-O-methyltransferase     

Resolution of pheromone pulses in receptor cells of Antheraea polyphemus at different temperatures

The ability of pheromone receptor cells of male Antheraea polyphemus (Saturniidae) to resolve stimulus pulses was determined at different temperatures (8°, 18°, 28°C). The cells were stimulated by repeated 20-ms puffs of the pheromone components (E, Z)-6, 11-hexadecadienyl acetate and (E, Z)-6,11-hexadecadienal. At higher temperatures, higher frequencies of stimulus pulses were resolved by the nerve-impulse response: about 1.25 pulses per second at 8°C, 2.5 pulses/s at 18°C and 5 pulses/s at 28°C. The decreased ability of receptor cells to resolve stimulus pulses at low temperatures may reduce the male moth's chance of reaching the pheromone source. The peak nerve-impulse frequency increased whereas the duration of nerve-impulse responses to single stimulus pulses decreased at higher temperatures. At a given temperature and stimulus intensity the peak nerveimpulse frequency decreased with shorter intervals between the stimulus pulses, but the duration of the responses remained almost constant. The time needed for recovery from adaptation caused by a single stimulus pulse was longer at lower temperatures. The aldehyde receptor cell recovered more quickly than the acetate cell. At low stimulus concentration, the resolution ability of the acetate cell was strongly decreased, whereas in the aldehyde cell it was only slightly impaired.     

Cyclic nucleotide-gated channels are involved in phototransduction of dermal photoreceptors in Lymnaea stagnalis

Dermal photoreceptors in the pond snail Lymnaea stagnalis mediate the whole-body withdrawal response, including pneumostome closure, elicited by a shadow passing over the pneumostome area. The pneumostome closure response is part of the defense reaction in Lymnaea. The shadow or ‘light-off’ stimulus elicits activity in a higher order interneuron, RPeD11, which has a major role in mediating defensive withdrawal behavior elicited by noxious or threatening stimuli. Here, we tested our hypothesis that cyclic nucleotide-gated (CNG) channels are involved in the dermal photoreceptor-mediated transduction of the shadow stimulus. The response to the shadow stimulus recorded in RPeD11 was abolished by 500 μM cis-diltiazem, which blocks cGMP-activated conductance of CNG channels. On the other hand, the shadow response elicited in RPeD11 was not blocked by 2-amino ethyldiphenyl borate (2-APB), a transient receptor potential (TRP) channel blocker. Consistent with the electrophysiologic data, cis-diltiazem blocked the shadow-evoked withdrawal response, whereas 2-APB did not block the withdrawal response evoked by the shadow stimulus in intact freely behaving Lymnaea. Together, these findings support the hypothesis that the second messenger in dermal photoreceptors involves CNG and not TRP channels.     

Hatching of Daphnia sexual eggs. II. The effect of age and a second stimulus

• 1 We examined the effect of age on the hatching response of Daphnia magna sexual eggs of specific families. For old eggs (>2 years), hatching characteristics were compared at two storage temperatures (4°C and 20°C). Also, the hatching response after a second dark incubation and subsequent incubation under conditions favourable for hatching was compared with that after the first stimulus.
• 2 Daphnia sexual eggs were found to remain viable for several (at least 4.5) years. The effect of age on the hatching rate was family dependent. At least in some families, hatching rate was higher for old (>2 years) than for young (<5 months) eggs. Low temperature (4°C) during dark incubation resulted in a higher hatching rate compared with incubation at 20°C.
• 3 The application of a second hatching stimulus resulted in a renewed hatching response. The overall hatching rate after the second stimulus was, however, lower than that of the first stimulus.
• 4 More than 80% of the hatchlings of young eggs appeared on Day 3 or 4, with minor between-family differences in time distribution of hatching. The timing of the response to hatching stimuli was more variable in old than in young eggs, with the average time at hatching being 6.4 instead of 4.0 days. The response to the application of hatching stimuli was also slower after the second stimulus compared with the first stimulus.

     

Facial nerve sensory responses recorded from the geniculate ganglion ofGallus gallus var.domesticus

Summary The extracellular responses of single sensory afferent cell bodies were recorded from the geniculate ganglion of the chicken following chemical, mechanical and thermal stimulation of the oral cavity using glass coated tungsten microelectrodes. Forty eight chemoreceptive units were identified from the anterior and posterior palate, and from the anterior mandibular area of the lower jaw. Their response characteristics to tyrode Ringer solution, distilled water, 0.05M hydrochloric acid, 0.5M sodium chloride, 1M fructose and 0.05M quinine hydrochloride were investigated. Only 5 units responded to a single stimulus and all of the other units responded to 2 or more stimuli. Thirty seven of the units which did not show single stimulus specificity did however respond best to one of the stimuli tested. The firing rates of these chemoresponsive units was slow, they showed little or no spontaneous activity and showed variable response patterns.Rapidly adapting and slowly adapting mechanoreceptors were also identified together with thermoreceptors (cold and warm units) and ear units.The results show that the facial nerve plays the major role in gustatory physiology of the chicken and these results are discussed in relation to the mammalian gustatory system.Abbreviations AMA anterior mandibular area - AP anterior palate - PP posterior palate - QHCl quinine hydrochloride     

Vibrational sensitivity of the wing of the pigeon (Columba livia) — a study using heart rate conditioning

Summary The vibrational sensitivity of awake pigeons was tested with the heart rate conditioning method. This method proved to be a very sensitive instrument for the behavioural measurement of the pigeon's sensitivity to mechanical stimuli.Sine wave vibrational stimuli between 50 and 2000 Hz were applied to the 1st, 7th and 16th primary feathers of the wing. The resulting threshold curves were U- or V-shaped with 3 characteristics: (i) The frequency of best response was either 800 or 900 Hz. (ii) Within the broad frequency range of vibrational sensitivity (50 to 2000 Hz) the sensitivity was extremely high at the best frequency: threshold amplitudes lay between 0.5 and 0.09 m. (iii) The threshold curves showed very sharp tuning at best frequency with bandwidths between 0.3 and 0.7 octaves (measured at best frequency 10fold above threshold). The functional meaning of the characteristic vibrational sensitivity of the wing for flight control is discussed; it is interpreted as an adaptation to special situations occurring during flight.Abbreviations CR conditioned response - CS conditioned stimulus - ECG electrocardiogram - HC(s) Herbst corpuscle(s) - UCS unconditioned stimulus All experiments were carried out at the Ruhr-Universität Bochum, Lehrstuhl für Allgemeine Zoologie     

The proboscis extention response and tarsal and labellar chemosensory hairs in the blowfly

Summary Four types of tarsal chemosensory hairs proposed by Grabowski and Dethier (1954) in the blowfly,Phormia regina, were reclassified into the following six types:A-,B ₁-,B ₂-,B ₃-,C- andD-type, based on the electrophysiological results. As for the labellar hairs, the results obtained by Wilczek (1967) agreed well with those in this work. The concentration-response curves of sugar receptors inB ₂-, andD-type of tarsal hairs and all types of labellar hairs for sugar stimulation were compared in relation to the regression of the acceptance threshold in the proboscis extention response of the blowflies starved for twenty four hours. The initial step of this response could be considered to be triggered mainly by about twelve impulses of every sugar receptor unD-type hairs during initial 0.1 sec after stimulus.     

Acoustic modulation of neural activity in the preoptic area and ventral hypothalamus of the green treefrog (Hyla cinerea)

Summary Responses of neurons in the preoptic area and ventral hypothalamus to conspecific mating calls or white noise bursts were examined in male green treefrogs (Hyla cinerea) during different seasons. In the winter, 34.3% of preoptic neurons and 46.7% of ventral hypothalamic cells demonstrated significant changes in activity level during presentation of a conspecific mating call. In contrast, only 13.3% of preoptic units and 16.7% of ventral hypothalamic cells responded to the white noise. The percentage of preoptic and hypothalamic units responding to the advertisement call did not differ significantly during the summer breeding season. Type I units exhibited a dramatic increase in activity during acoustic stimulation followed by a rapid return to baseline activity levels after stimulus offset. Type II cells showed a robust activity increase during stimulation, but maintained an intermediate activity level after stimulus offset. In the preoptic area, a third response type exhibited suppressed activity during acoustic stimulation. Although seasonal condition did not alter the percentage of acoustically responsive units within either nucleus, the proportion of Type I units in the ventral hypothalamus was greatest during the summer.Abbreviations MC mating call - NS no stimulus - POA preoptic area - VH ventral hypothalamus - WN white noise     

Adaptation and temporal characteristics of the insect visual response

Summary The effects of light adaptation on temporal characteristics of the electroretinogram were studied in two species of diurnal insects. Latency and time to reach peak amplitude (T _m ) of the initial deflection of the ERG were the temporal measures used. The experimental regime consisted of repeatedly light-adapting the eye with a conditioning stimulus (S ₁ and determining the effects of eachS ₁ on the response to a test stimulus (S ₂). The compound eyes of the flesh flySarcophaga bullata, and the milkweed bug,Oncopeltus fasciatus, were compared since they differ substantially in ERG waveform and latency of response.The latency to a test stimulus (S ₂) decreased nearly linearly with the logarithm of the intensity and/or duration ofS ₁. Increases in adapting stimulus (S ₁) durations beyond about 10 sec resulted in only slight temporal changes in the response toS ₂. For 3 log units ofS ₁ quantal input, the changes inS ₂ latency andT _m generally follow the Bunsen-Roscoe law.The persistence of the effects of light adaptation on the latency of response depended upon the quantity of light in the adapting stimulus. Following cessation of the light-adapting stimulus, a lag time was observed during which the latency remained near the light-adapted value for several seconds before returning to the dark-adapted state.We would like to thank Professors J. F. Case, F. Crescitelli and R. K. Josephson for reading and commenting upon this work Mr. G. Stone and Miss D. Martinez provided helpful technical assistance. We also want to thank Professor H. A. Schneiderman who generously provided experimental animals. This research was supported in part by a Grant-in-Aid from the Society of Sigma Xi.     

Thermal stimulation of exposed skin area influences behavioral thermoregulation in pigeons

Summary Pigeons were trained to work instrumentally for thermal reinforcement under ambient heat and cold loads. Facial or breast skin temperature was selectively altered by means of air-perfused thermodes. Facial stimulation with temperatures in the normally occurring range resulted in changes of instrumental response rate, accompanied by stimulus opposing deviations of core temperature (Fig. 5). Breast skin stimulations with the same stimulation amplitudes also affected behavioral thermoregulation, but without changing core temperature. Small temperature changes, as naturally occur at feathered breast skin, had no effect on response rate. Behavioral adjustments occurring within 15 s in response to altering either ambient load temperature or facial temperature locally (Fig. 6), support the hypothesis that the face represents a site driving short term behavioral adjustments to ambient disturbances.Abbreviations RF reinforcement(s) - T _a temporal mean of ambient temperature - T _load load temperature - T _c (colonic) core temperature - T _s skin temperature - T _s(v) ventral skin temperature - T _s(d) dorsal skin temperature - T _ax axilla temperature     

Activity of Sphaerotheca breviceps tadpoles in response to chemical cues of the predaceous tadpoles Hoplobatrachus tigerinus

Tadpoles of Sphaerotheca breviceps raised in the laboratory from the egg stage, and hence lacking prior experience of a predator or its odors, were tested to examine their responses to a predator’s (tadpoles of Hoplobatrachus tigerinus) water-borne chemical cues. The stimulus solution was obtained following 24 h of rearing tadpoles of H. tigerinus (one tadpole per 200 mL water) that were not fed during this period. Upon exposure to the stimulus solution the activity of S. breviceps tadpoles decreased by about 90% within 5 min. Their resting period increased significantly over baseline activity, whereas the swimming period, distance traversed, and swimming spurts declined. However, whenever a test tadpole moved, its swimming velocity was high in response to stimulus solution. The antipredatory responses declined with increase in time of storage of the stimulus solution, indicating decay of the predator’s chemical cues. The findings suggest that (1) antipredator defense strategies of S. breviceps do not require prior experience of predators, (2) the predator’s chemical cues are labile in nature, and (3) the response of prey tadpoles to such cues is similar to reported behavior of anuran tadpoles in response to real predators and alarm cues.     

Sensory cues for the gradual frequency fall responses of the gymnotiform electric fish, Rhamphichthys rostratus

The sensory cues for a less known form of frequency shifting behavior, gradual frequency falls, of electric organ discharges (EODs) in a pulse-type gymnotiform electric fish, Rhamphichthys rostratus, were identified. We found that the gradual frequency fall occurs independently of more commonly observed momentary phase shifting behavior, and is due to perturbation of sensory feedback of the fish's own EODs by EODs of neighboring fish. The following components were identified as essential features in the signal mixture of the fish's own and the neighbor's EOD pulses: (1) the neighbor's pulses must be placed within a few millisecond of the fish's own pulses, (2) the neighbor's pulses, presented singly at low frequencies (0.2–4 Hz), were sufficient, (3) the frequency of individual pulse presentation must be below 4 Hz, (4) amplitude modulation of the sensory feedback of the fish's own pulses induced by such insertions of the neighbor's pulses must contain a high frequency component: sinusoidal amplitude modulation of the fish's own EOD feedback at these low frequencies does not induce gradual frequency falls. Differential stimulation across body surfaces, which is required for the jamming avoidance response (JAR) of wave-type gymnotiform electric fish, was not necessary for this behavior. We propose a cascade of high-pass and low-pass frequency filters within the amplitude processing pathway in the central nervous system as the mechanism of the gradual frequency fall response.Abbreviations EOD electric organ discharge - f frequency of EOD or pacemaker command signal - JAR jamming avoidance response - S ₁ stimulus mimicking fish's own EOD - f ₁ frequency of S₁ - S ₂ stimulus mimicking neighbor's EOD - f ₂ frequency of S₂     

Tracking the startle response of guppies Poecilia reticulata in three dimensions

A three‐dimensional analysis of startle behaviours of guppies Poecilia reticulata, in dyads or alone, from two populations that show distinct differences in shoaling behaviour was performed. During the first few seconds after a startling stimulus, changes in behaviour, which could be critical if an individual is to survive a predatory attack, and the interactions between pairs of P. reticulata were examined. The enhanced social interactions immediately after the stimulus, as a proxy for shoaling behaviour, and their dissipation were quantified. Social (individuals tested in dyads) v. asocial (tested alone) responses to the startling stimulus were also compared. The three‐dimensional reconstruction, from a two‐camera, high‐frame‐rate tracking system allowed for the tracking of the individuals' speed and speed recovery and, for P. reticulata in dyads, interindividual distance and orientation. For the dyads from the high‐predation population, the closer the individuals were to each other, the more likely they were to be parallel, but no correlation was found for the low‐predation P. reticulata. The startle response of P. reticulata comprised the following sequence: freezing, darting and skittering and recovery to pre‐stimulus swimming behaviour. Upon repeated encounters with the stimulus, a reduced shoaling and startle response was observed, although the rate of reduction was faster in P. reticulata from the high‐predation population than those from the low‐predation population. The results are discussed in light of what is known about the anti‐predator behaviour of this species.