How greater mouse-eared bats deal with ambiguous echoic scenes.

Echolocating bats have to assign the received echoes to the correct call that generated them. Failing to do so will result in the perception of virtual targets that are positioned where there is no actual target. The assignment of echoes to the emitted calls can be ambiguous especially if the pulse intervals between calls are short and kept constant. Here, we present first evidence that greater mouse-eared bats deal with ambiguity by changing the pulse interval more often, in particular by reducing the number of calls in the terminal group before landing. This strategy separates virtual targets from real ones according to their change in position. Real targets will always remain in a constant position, and virtual targets will jitter back and forth according to the change in the time interval.

Carbachol injections into the nucleus accumbens disrupt acquisition and expression of fear-potentiated startle and freezing in rats.

The nucleus accumbens is involved in different types of emotional learning, ranging from appetitive instrumental learning to Pavlovian fear conditioning. In previous studies, we found that temporary inactivation of the nucleus accumbens blocked both the acquisition and expression of conditioned fear. This was not due to altered dopaminergic activity as we have also found that intra-nucleus accumbens infusions of the dopamine agonist amphetamine do not affect either the acquisition or the expression of conditioned fear. Therefore, in the present study we examined whether cholinergic activity in the nucleus accumbens is involved in the acquisition and expression of conditioned fear. Specifically, the effect of intra-nucleus accumbens infusions of the unselective cholinergic agonist carbachol on the acquisition and expression of conditioned fear was assessed. Across several experiments, we measured fear to visual and acoustic conditioned stimuli and to the experimental context. Further, two different measures of conditioned fear were recorded: fear potentiation of startle and freezing. Intra-nucleus accumbens carbachol infusions disrupted acquisition as well as expression of conditioned fear, regardless of the modality of the fear-eliciting stimulus or of the specific measure of conditioned fear. This disruption of conditioned fear was not simply a by-product of enhanced motor activity which also occurred after intra-nucleus accumbens carbachol infusions. Interestingly, despite the substantial effect of intra-nucleus accumbens carbachol on expression of conditioned fear, the results of the final experiment suggest that these rats extinguish similarly to control rats. Taken together, the present results indicate that acetylcholine within the nucleus accumbens is important for the learning and retrieval of conditioned fear.

Echolocation by the barbastelle bat, Barbastella barbastellus.

When searching for insects along edges, Barbastella barbastellus alternated between two signal types. Type-2 signals had durations around 6 ms and were composed of an initial shallowly downward frequency modulated component, starting at about 45 kHz and followed by a shorter more steeply modulated component that ended at about 32 kHz. Type-1 signals were rather stereotyped with durations around 2.5 ms and a very short rise time. They covered an approximately 8 kHz-wide frequency band positioned just below the 12-15 kHz-wide frequency band of type-2 signals, with no or small frequency overlap. In the recordings, type-1 signals almost had always a higher amplitude than type-2 signals, at least partly caused by head movements. Assuming that signal structure reflects function, we hypothesize that type-2 signals have the same adaptive value as the signals with a broadband and narrowband component of other vespertilionids, but with a reverse arrangement of the signal elements. Like the broadband component of the type-2 signals, type-1 signals are well suited to localize background targets. Thus, the localization component may be distributed among two signals separated in time, which has the advantage that both signals can be varied independently in the direction of emission and in amplitude.

Increased sensitization of acoustic startle response in spasmodic mice with a mutation of the glycine receptor alpha1-subunit gene.

The spontaneous mutant mouse spasmodic (spd) carries a missense mutation affecting the glycine receptor alpha1-subunit gene. This results in a decreased binding affinity to glycine. Spd mutants show exaggerated acoustic startle responses (ASR). The present study sought to elucidate whether this increased ASR is due to a changed auditory processing or to stronger motor output resulting from a disinhibited motor system or, alternatively, to changes in modulatory influences on the startle pathway, namely in the mechanisms underlying habituation and sensitization. We found that in homozygous spd/spd mutants the startle threshold was lower, and the recorded slope of input/output (i/o) function, which reflects the relation between sensory input and motor output, was steeper. During repetitive presentation of high sound pressure level (SPL) startle stimuli (25 dB above startle threshold), ASR amplitudes did not decrease in spd/spd mutants as they do in the wildtype. In contrast, ASR amplitudes decreased when low SPL startle stimuli were presented. Footshocks presented after high SPL startle stimuli did not cause a further increase in ASR amplitudes of spd/spd mutants as in the wildtype. In heterozygous spd/+ mutants all these parameters were between those of spd/spd mutants and wildtype mice but closer to those of the wildtype. The steeper slope of i/o function in spd/spd mutants may be caused by both an increased sensory input and an increased motor output. The altered course of ASR amplitudes during repetitive stimulation and the deficit in additional footshock sensitization, however, can only be explained by an increased sensitization level in the spd/spd mutants. In accordance with the "dual process theory" strong sensitization evoked by high SPL startle stimuli supposedly counteracts habituation, leading to a constant high ASR amplitude. Furthermore, additional footshock sensitization is prevented. The increased sensitization level may be due to a change in auditory processing leading to a stronger sensitizing effect of the startle stimuli with high SPL. Alternatively, glycinergic tonic inhibition of sensitizing structures (e.g. the amygdala) in the wildtype may be diminished in spd/spd mutants, thus leading to a high sensitization level.

The acoustic advantage of hunting at low heights above water: behavioural experiments on the European 'trawling' bats Myotis capaccinii, M. dasycneme and M. daubentonii.

We have demonstrated in behavioural experiments that success in capturing prey from surfaces in 'trawling Myotis' (Leuconoë-type) depends on the acoustic properties of the surface on which the prey is presented. Two types of surface structure were ensonified with artificial bat signals to probe their acoustic characteristics. We have shown that perception of prey by echolocation is easier if the prey is presented on a smooth surface (such as calm water) than if it is presented on a structured surface (such as vegetation or the ground). This is because the smooth surface reflects a much lower level of clutter echoes than the structured one if ensonified at an angle typical for bats foraging low over water. The ensonification experiments revealed that the sound pressure level of the echo was even higher for mealworms on a smooth surface than for mealworms suspended in air. This might be because waves travelling via the surface also contribute to the echo (e.g. reflection from the surface to the mealworm, back to the surface and then to the receiver). From the behavioural experiments, we conclude that 'trawling Myotis' take isolated objects on smooth (water) surfaces for prey. Those objects reflect isolated, stationary acoustic glints back to the echolocating bats. Conversely, 'trawling Myotis' will not recognise prey if prey echoes are embedded in numerous clutter echoes. We have demonstrated marked similarities between the three European 'trawling Myotis' species M. dasycneme, M. daubentonii and M. capaccinii in echolocation behaviour, search image, foraging strategy and prey perception. We propose that a combination of prey abundance and acoustic advantages could have led to repeated and convergent evolution of 'trawling' bats in different parts of the world.

Role of muscles accumbens dopamine D1 and D2 receptors in instrumental and Pavlovian paradigms of conditioned reward.

RATIONALE: This study investigated the role of nucleus accumbens dopamine D1 and D2 receptors in two different paradigms of conditioned reward. OBJECTIVE: We addressed the question whether accumbal dopamine is important for the motor or for the motivational components of reward. METHODS: We compared the effects of intra-accumbal infusion of the dopamine D1 receptor antagonist SCH23390 (0.3, 1.0, 3.0 microg) and the D2 receptor antagonist sulpiride (0.3, 1.0, 3.0 microg) on conditioned lever pressing for food, with the effects on the inhibition of the startle response by a conditioned reward signal. RESULTS: Both the D1 and the D2 antagonist dose-dependently attenuated conditioned lever pressing for reward under a fixed-ratio of responding and increased the consumption of freely available lab chow. However, the preference for freely available pellets, and the attenuation of the startle response in the presence of a conditioned stimulus predicting reward were not impaired by blockade of accumbal dopamine receptors. CONCLUSIONS: Our data support the idea that dopamine in the nucleus accumbens is necessary for instrumental response selection in the context of reward rather than for the mere motor performance of behavior or for the evaluation of the hedonic properties of rewarding stimuli.

Acoustic flow perception in cf-bats: extraction of parameters.

The narrow-band portions of the echolocation pulses seen in cf-bats are a hypothetical substrate for target localization. This localization could be based on estimates of echo envelope amplitude and carrier frequency together with their derivatives. Evaluation of these parameters is referred to as "acoustic flow" in loose analogy to optic flow. It is assessed whether the requirements for this task may be reconciled with known principles of auditory function. For the evaluation of a single echo, this seems to be the case: auditory filter shapes provide sufficient frequency resolution; at the same time envelopes are preserved well and some noise removal is achieved. Nevertheless, should bats not be endowed with additional capabilities for noise removal, analysis of acoustic flow would be limited to favorable signal-to-noise ratios. Multiple, temporally overlapping echoes are probable in any realistic echolocation scenario. In this case, additional auditory processing steps have to be postulated, which allow simultaneous estimation of multiple carrier frequencies and reduction of demodulation distortions.

Lesions of the rat piriform cortex prevent long-lasting sensorimotor gating deficits induced by stimulation of the ventral hippocampus.

Prepulse inhibition (PPI) is a cross-species operational measure of sensorimotor gating. Reduced PPI is found in schizophrenics and can be induced experimentally in rats. Stimulation of the rat ventral hippocampus (VH) with N-methyl-D-aspartate (NMDA) results in long-lasting PPI deficits (carry-over effect). Since we have previously shown that this carry-over effect was accompanied by increased expression of c-Fos in the piriform cortex (PIR), we here tested the effects of lesions of the PIR on PPI after stimulation of the VH. PIR lesioned rats still showed disruption of PPI after injection of NMDA into the VH. However, the carry-over effect observed in controls was prevented by PIR lesions. These data suggest that the PIR is important for long-lasting alterations in brain functioning leading to impaired sensorimotor gating.

Interaction between acoustic and electric sensitization of the acoustic startle response in rats.

Sensitization is the general increase of responsiveness observed after aversive stimulation. Usually footshocks are used as aversive stimuli. According to the 'Dual Process Theory' by Groves and Thompson. Psychol. Rev. 1970;77:419-450, not only additional aversive stimuli but also the response-eliciting stimuli themselves have a sensitizing effect, the degree of sensitization depending upon the stimulus intensity. We tested this suggestion in the footshock sensitization paradigm of the acoustic startle response (ASR): (1) High SPL (sound pressure level) acoustic stimuli (119 dB SPL) presented instead of footshocks also elicited strong sensitization. (2) While footshocks presented after startle stimuli with low SPL (95 dB) were able to produce a strong further sensitization of the ASR, footshocks presented after startle stimuli with high SPL (110 dB) only caused a minor sensitization of the ASR. (3) Diazepam (3 mg/kg i.p.) decreased ASR to high SPL (115 dB) stimuli. In this case footshocks elicited significant sensitization of the ASR despite intense startle stimuli. The present results support the 'Dual Process Theory'. Furthermore we could show that acoustic and footshock sensitization interact. We therefore suggest that both, acoustic and footshock sensitization, are mediated partly via the same neural circuitry.

Acoustic flow perception in cf-bats: properties of the available cues.

Signal design in cf-bats is hypothesized to be commensurate with the evaluation of time-variant echo parameters, imposed by changes in the sound channel occurring as the bat flies by a target. Two such parameters, the proportional changes in Doppler frequency and sound pressure amplitude, are surveyed, employing a simplified acoustic model in order to assess their fitness for target localization given a translational movement within a plane. This is accomplished by considering the properties of the scalar fields given by the value of these putative sensory variables as a function of position in a plane. The considered criteria are: existence and extent of ambiguity areas (i.e., multiple solutions for target position), magnitude of the variables (relevant with regard to perceptual thresholds), as well as magnitude and orthogonality of the gradients (relevant to localization accuracy). It is concluded that these properties render the considered variables compatible with gross judgements of target position. This may be sufficient for behavioral contexts like obstacle avoidance, where adoption of suitable safety margins could compensate for the variance and bias associated with estimates of target location.

Echo SPL, training experience, and experimental procedure influence the ranging performance in the big brown bat, Eptesicus fuscus.

Four Eptesicus fuscus were trained in a range discrimination experiment to choose the closer of two phantom targets. Echo attenuation was roving between trials returning echoes ranging from -10 dB to -50 dB SPL (sound pressure level) relative to emission SPL. Discrimination thresholds were determined. After sufficient training, ranging performance was stable and about the same in the range between -20 dB and -50 dB with range difference thresholds around 300 microseconds. At -10 dB, performance was poor even after long training. After additional training at a constant relative echo SPL of -30 dB and a delay difference of 300 microseconds the performance measured with roving echo SPL improved at all relative echo SPL between -20 dB and -50 dB but not at -10 dB. The new experimental procedure improved the performance by additional learning, and the bats generalized over a wide range of relative echo SPL. Threshold improved to 100 microseconds when measured at a constant relative echo SPL of -30 dB, again indicating the influence of the experimental procedure. In correspondence to neurophysiological data the ranging performance deteriorates if the echo SPL is close to the emission SPL. Signal duration and emission SPL were variable during range discrimination.

Induction of Fos-protein in the forebrain and disruption of sensorimotor gating following N-methyl-D-aspartate infusion into the ventral hippocampus of the rat.

Several neuropsychiatric disorders, including schizophrenia, are characterized by sensorimotor gating deficits. Prepulse inhibition of the acoustic startle response is an operational measure assessing sensorimotor gating and has been found to be reduced in schizophrenic patients. Much attention has therefore been paid to the neuronal mechanisms underlying the disruption of prepulse inhibition. The activity of limbic forebrain structures such as the septohippocampal system, the prefrontal cortex, and the nucleus accumbens has been the main focus of recent research into the regulation of prepulse inhibition in rats. We here provide a functional anatomical picture of forebrain structures probably involved in the regulation of prepulse inhibition. Stimulation of the ventral hippocampus with a subconvulsive dose of N-methyl-D-aspartate caused a significant and long-lasting disruption of prepulse inhibition. Immunostaining of the c-Fos protein revealed a characteristic pattern of neuronal activity in various forebrain areas, including the nucleus accumbens and different frontal cortical areas after hippocampal stimulation. Based on the present findings, we conclude that the overactivity within a network of cortico-limbic forebrain structures compromises the normal processing of sensory stimuli by disrupting a neuronal filter mechanism. Interestingly, there is a considerable overlap between the pattern of neuronal activity observed in our study and the brain pathology in schizophrenics reported in the literature.

Echolocation signals of the greater horseshoe bat (Rhinolophus ferrumequinum) in transfer flight and during landing.

Echolocation signals of horseshoe bats (Rhinolophidae) consist of a relatively long component of constant frequency (CF) which is preceded by an initial frequency-modulated (iFM) component and followed by a terminal frequency-modulated (tFM) component. To examine the role of these components in echolocation, four bats were trained to fly from a perch to a landing bar. A dual camera system allowed reconstruction of the flight paths in three dimensions. Echolocation signals were recorded, analyzed, and correlated with the flight behavior of the bats. It was confirmed that during flight the bats compensate the Doppler shifts which are produced by their own flight movement. In free flight they emit per wing beat one single signal of long duration, with little variation in the three signal components. In approach flight the bats reduce pulse duration and interval with decreasing target range. The iFM is not varied with respect to target range, suggesting that this component plays little role in the processing of echolocating a target of interest. The bandwidth of the tFM component is increased while its duration is shortened in proportion to decreasing target range, so that the signal-echo overlap of the FM component is avoided down to a target distance of 15 cm. These concurrent changes suggest that the tFM component is used for ranging. During the last 60 cm of the approach the bats compensated for the increase of echo SPL by lowering the emission level of the CF component by 6-9 dB and that of the tFM component by 9-11 dB per halving of range. The specific signal structure of horseshoe bats is discussed as an adaptation for the hunting of fluttering insects in highly cluttered environments.

Effect of the middle ear reflex on sound transmission to the inner ear of rat.

The effect of the acoustic middle ear reflex (MER) was quantified using electrodes chronically implanted in the middle ears of rats. Cochlear microphonics (CM) and middle ear muscle EMG were measured under light Ketamin anesthesia after stimulation with tone pulses of 5-20 kHz ranging between 75 and 120 dB SPL. With increasing intensity, the CM measured before the onset of the MER increased to a maximum amplitude and then decreased with higher SPLs. At 10 kHz this maximum was reached at 95 dB SPL, for other stimulus frequencies at higher SPLs. After a latency of 10-20 ms, CM to 10 kHz stimuli of 80-95 dB SPL were decreased by the attenuating action of the MER. The lowest threshold of the MER was also measured at 10 kHz (77 dB SPL in the mean). To stimuli greater than 100 dB SPL after a latency of 6-10 ms, the CM amplitude was increased. That this CM increase to intense stimuli is caused by the action of the MER was confirmed by control experiments such as cutting the tendons of the middle ear muscles. The CM decrease to stimuli below 100 dB SPL, as well as the increase to very intense stimuli, can be explained by sound attenuation caused by the MER, together with the nonlinear dependence of CM amplitude on stimulus level. The observed shift of the maxima of the CM input-output function by the MER to higher stimulus levels probably indicates an increase of the dynamic range of the ear.

Corticotropin-releasing factor in the caudal pontine reticular nucleus mediates the expression of fear-potentiated startle in the rat.

The fear-potentiated startle paradigm is a valuable model for the investigation of the neuronal basis of fear. Previous studies have demonstrated that the neuropeptide corticotropin-releasing factor (CRF) plays an important role in fear-related processes, notably in the potentiation of the acoustic startle response. The present study investigated the role in fear-potentiated startle of CRF in the caudal pontine reticular nucleus, a brain nucleus that mediates the acoustic startle response. First, we showed that the central nucleus of the amygdala gives rise to a CRFergic projection to the caudal pontine reticular nucleus. In the second experiment, we iontophoretically applied CRF to caudal pontine reticular nucleus neurons and extracellularly recorded the activity of these neurons. CRF had a mainly excitatory effect on the tone-evoked activity of the neurons. In our third experiment, we injected the CRF antagonist alpha-helical CRF into the caudal pontine reticular nucleus of awake rats. Here, alpha-helical CRF dose-dependently blocked fear-potentiated startle, but had no effect on the baseline startle amplitude. The present results show that CRF-containing neurons which project from the central nucleus to the caudal pontine reticular nucleus are important for the enhancement of startle by fear, and further characterize the hypothetical neuronal circuitry underlying the expression of fear-potentiated startle.

The acoustic startle response in rats--circuits mediating evocation, inhibition and potentiation.

This review describes the neuronal mechanisms underlying the mediation and modulation of the acoustic startle response (ASR) in rats. The combination of anatomical, physiological and behavioral methods has identified pathways which mediate and modulate the ASR. The ASR is mediated by a relatively simple, oligosynaptic pathway located in the lower brainstem which activates spinal and cranial motor neurons. An important element of the pathway which mediates the ASR is the caudal nucleus of the pontine reticular formation (PnC). Interestingly, this nucleus is also the target of input from various brain nuclei which are involved in the modulation (e.g. fear-potentiation, sensitization, habituation, prepulse inhibition and pleasure-attenuation) of the ASR. Hence, the PnC can be described as a sensorimotor interface, where the transition of sensory input into the motor output can be directly influenced by excitatory or inhibitory afferents. On the basis of these facts we conclude that the ASR may be a valuable model for the study of general principles of sensorimotor-motivational information processing at the behavioral and neurophysiological level in mammals.

NMDA receptors in the pontine brainstem are necessary for fear potentiation of the startle response.

The fear-potentiated startle model in rats is a valuable animal test for the investigation of the neural and neurochemical basis of fear. In this model, rats are trained to associate a neutral stimulus with an aversive stimulus, so that after conditioning the conditioned stimulus alone elicits a state of fear leading to an exaggerated acoustic startle response. The fear-potentiated startle model does not require instrumental responding for the indication of states of fear. The acoustic startle response is mediated by a simple brainstem circuit, with the caudal pontine reticular nucleus as an interface that receives input from startle-enhancing circuits. In the present study, we tested the hypothesis that N-methyl-D-aspartate (NMDA) receptors on neurones of the caudal pontine reticular nucleus are involved in the mediation of fear-potentiated startle. After fear-conditioning, we injected the NMDA receptor antagonist DL-2-amino-5-phosphonopentanoic acid (AP-5), into the caudal pontine reticular nucleus of awake rats and tested the effect on the expression of fear-potentiated startle. Injections of AP-5 (0.125-0.5 nmol) into the caudal pontine reticular nucleus dose dependently attenuated fear-potentiated startle without affecting the baseline amplitude of the acoustic startle response. The results suggests that, in the caudal pontine reticular nucleus, glutamate may mediate fear-potentiated startle via NMDA receptors.

Lesions of the amygdala do not affect the enhancement of the acoustic startle response by background noise.

The acoustic startle response (ASR) is enhanced in the presence of loud background noise. We examined whether or not this increase of response strength is mediated by the amygdala, which is known to be involved in various phenomena of enhancement of the ASR. To achieve this aim, we tested whether or not amygdaloid lesions with the excitotoxin N-methyl-D-aspartate (NMDA) would abolish the enhancement of the ASR by background noise in 13 Wistar rats. Loss of foot-shock sensitization in these rats, as well as histological evaluation, proved the successful destruction of the amygdala. However, the enhancement by background noise of the ASR, which was observed in sham-operated controls, was not affected in amygdala-lesioned rats. Therefore, we conclude that the background noise facilitation does not involve emotional components that are mediated by the amygdala. On the basis of these findings, we differentiate between the startle-enhancing effect of background noise and the amygdala-mediated effect of foot shocks on the ASR.

Habituation and sensitization of the acoustic startle response in rats: amplitude, threshold, and latency measures.

The amplitude of the acoustic startle response habituates to repetitive stimulation. The input and output of the startle system were measured to determine if the decrease in startle amplitude during repetitive stimulation is due to an increase in the startle threshold. Two experimental approaches were used in 35 Sprague-Dawley rats to probe the relationship between the input (the sound pressure level of the stimulus) and the behavioral output (startle amplitude). The results show that the minimum threshold for a response does not change during habituation; rather, the slope of the dependence of startle amplitude on stimulus level decreases. Because habituation does not influence startle threshold we propose that the site for habituation is located in the neural circuitry downstream from the site for startle threshold. Besides amplitude and threshold, as an additional parameter we measured startle latency. In general, the latency of the acoustic startle response is negatively correlated with the response amplitude. This correlation has been repeatedly shown, therefore one would expect a latency increase during the amplitude decrease caused by habituation. However, the latency of the startle reaction also decreased during the course of repetitive stimulation. According to the dual process theory of habituation, a stimulus has both a response-decreasing, i. e., habituating, as well as a response-increasing, i.e., sensitizing, influence on a behavior (Groves & Thompson, 1970). Our explanation of the present results is that startle amplitude is reduced following repetitive stimulation because it is mainly influenced by habituation; latency, however, is shortened because it is mainly influenced by sensitization.

Somatostatin in the pontine reticular formation modulates fear potentiation of the acoustic startle response: an anatomical, electrophysiological, and behavioral study.

The amplitude of the acoustic startle response (ASP) in rats is increased in the presence of a cue that has previously been paired with an aversive stimulus such as a footshock. This phenomenon is called fear-potentiated startle and is a model to study the neuronal and neurochemical mechanisms of the acquisition and expression of fear. The present study investigated the role in fear-potentiated startle of somatostatin in the caudal pontine reticular nucleus (PnC) by a combination of anatomical, electrophysical, and behavioral methods. The PnC is an essential part of the primary startle circuit and is also the recipient of modulatory influences. First, we showed that the central gray (CG), which is involved in fear conditioning, is the main source of somatostatinergic input to the PnC. In the second experiment, we iontophoretically applied the somatostatin receptor agonist sandostatin on PnC neurons and extracellularly recorded the activity of PnC neurons. Sandostatin had no effect on tone-evoked or spontaneous activity, but markedly attenuated the increase of neuronal activity seen after the administration of glutamate. In our third experiment, we injected different doses of sandostatin into the PnC of awake rats. Sandostatin blocked fear potentiation of the ASR but had no effect on the baseline ASR amplitude. The present study indicates that the somatostatinergic projection from the CG to the PnC is important for the modulation of fear-potentiated startle. We present a possible neural circuitry for the expression of fear-potentiated startle based on these data and previous findings.