The role of a midbrain network in competitive stimulus selection

A midbrain network interacts with the well-known frontoparietal forebrain network to select stimuli for gaze and spatial attention. The midbrain network, containing the superior colliculus (SC; optic tectum, OT, in non-mammalian vertebrates) and the isthmic nuclei, helps evaluate the relative priorities of competing stimuli and encodes them in a topographic map of space. Behavioral experiments in monkeys demonstrate an essential contribution of the SC to stimulus selection when the relative priorities of competing stimuli are similar. Neurophysiological results from the owl OT demonstrate a neural correlate of this essential contribution of the SC/OT. The multi-layered, spatiotopic organization of the midbrain network lends itself to the analysis and modeling of the mechanisms underlying stimulus selection for gaze and spatial attention.     

Precognitive and cognitive elements in sound localization

Sound localization behavior is of great importance for an animal's survival. To localize a sound, animals have to detect a sound source and assign a location to it. In this review we discuss recent results on the underlying mechanisms and on modulatory influences in the barn owl, an auditory specialist with very well developed capabilities to localize sound. Information processing in the barn owl auditory pathway underlying the computations of detection and localization is well understood. This analysis of the sensory information primarily determines the following orienting behavior towards the sound source. However, orienting behavior may be modulated by cognitive (top-down) influences such as attention. We show how advanced stimulation techniques can be used to determine the importance of different cues for sound localization in quasi-realistic stimulation situations, how attentional influences can improve the response to behaviorally relevant stimuli, and how attention can modulate related neural responses. Taken together, these data indicate how sound localization might function in the usually complex natural environment.     

Behavioral guides for sensory neurophysiology

The study of natural behavior is important for understanding the coding schemes of sensory systems. The jamming avoidance response of the weakly electric fish Eigenmannia is an excellent example of a bottom–up approach, in which behavioral analyses guided neurophysiological studies. These studies started from the electroreceptive sense organs to the motor output consisting of pacemaker neurons. Going in the opposite direction, from the central nervous system to lower centers, is the characteristic of the top–down approach. Although this approach is perhaps more difficult than the bottom–up approach, it was successfully employed in the neuroethological analysis of sound localization in the barn owl. In the latter studies, high-order neurons selective for complex natural stimuli led to the discovery of neural pathways and networks responsible for the genesis of the stimulus selectivity. Comparison of Eigenmannia and barn owls, and their neural systems, has revealed similarities in network designs, such as parallel pathways and their convergence to produce stimulus selectivity necessary for detection of natural stimuli.     

Experimental evidence for olfactory predator recognition in wild mouse lemurs

Although primates have remarkable olfactory capabilities, their ability for olfactory predator recognition is still understudied. We investigated this cognitive ability in wild gray and golden-brown mouse lemurs (Microcebus murinus and M. ravelobensis) that were confronted with four different olfactory stimuli, derived from two Malagasy predators (fossa and barn owl) and two local nonpredator species (brown lemur and sifaka). The predator response was tested (1) in a systematic cage setup and (2) in a two-way choice experiment with two Sherman traps on platforms in the forest (stimulus trap vs. nonstimulus trap). For part 1, the study animals were housed in cages during habituation and 5 days of experiments. One stimulus was tested per night and was presented underneath a drinking bottle. The changes in the time spent close to the stimulus and the drinking time at the bottle were used as indicators of predator recognition. A timidity score was established by classifying the strength of the antipredator response during the experiment. The study animals spent significantly less time drinking and less time in the stimulus area when confronted with fossa odor compared with the other stimuli. The timidity score was significantly higher during the fossa stimulus compared with the nonpredator and the control stimuli. The two-way choice experiments revealed a complete avoidance of the fossa odor, which was not found with the other stimuli. Thus, wild mouse lemurs showed clear signs of olfactory predator recognition in the case of the fossa in both experiments, but no signs of avoidance to the other presented stimuli. The lack of owl avoidance may be explained by less or no aversive metabolites in the owl stimulus or by lower significance for olfactory recognition of aerial predators. Furthermore, the results showed slight differences between the two mouse lemur species that may be linked to differences in their ecology.     

Pupillary dilation response as an indicator of auditory discrimination in the barn owl

The pupil of an awake, untrained, head-restrained barn owl was found to dilate in response to sounds with a latency of about 25 ms. The magnitude of the dilation scaled with signal-to-noise ratio. The dilation response habituated when a sound was repeated, but recovered when stimulus frequency or location was changed. The magnitude of the recovered response was related to the degree to which habituating and novel stimuli differed and was therefore exploited to measure frequency and spatial discrimination. Frequency discrimination was examined by habituating the response to a reference tone at 3 kHz or 6 kHz and determining the minimum change in frequency required to induce recovery. We observed frequency discrimination of 125 Hz at 3 kHz and 250 Hz at 6 kHz – values comparable to those reported by others using an operant task. Spatial discrimination was assessed by habituating the response to a stimulus from one location and determining the minimum horizontal speaker separation required for recovery. This yielded the first measure of the minimum audible angle in the barn owl: 3° for broadband noise and 4.5° for narrowband noise. The acoustically evoked pupillary dilation is thus a promising indicator of auditory discrimination requiring neither training nor aversive stimuli. Accepted: 28 February 2000     

Restricted range of ocular accommodation in barn owls (Aves:Tytonidae)

Summary In an examination of the focusing abilities of 15 species of owls, the North American barn owl, Tyto alba pratincola (Bonaparte 1838), was an outstanding accommodator, having a range of accommodation exceeding 10 diopters (Murphy and Howland 1983). Using comparable methods, we examined the accommodation of 4 specimens of the Australian barn owl, Tyto alba delicatula (Gould 1837). We failed to elicit accommodation greater than two diopters, and most stimuli failed to evoke any discernable accommodation at all. Furthermore, examination of other Australian tytonid owls, the grass owl, T. longimembris, the sooty owl, T. tenebricosa, and both the mainland and Tasmanian subspecies of the masked owl, T. novaehollandiae novaehollandiae and T. novaehollandiae castanops, also failed to reveal anything but very moderate accommodative ranges. We conclude that the outstanding accommodative ability of the American barn owl is truly an exception to the modest accommodative abilities of the tytonid owls generally.     

Interspecific offspring killing in owls

In Baranya County (Southern Hungary), tawny owls (Strix aluco) and barn owls (Tyto alba) sequentially use the same nest boxes in a significant number of cases. A total of 460 broods were observed between 1996 and 2003 and, in 12 cases, whole broods of dead tawny owl chicks were registered that had apparently been killed. On investigating the reproductive life characteristics, population sizes, and frequency of killing in these two species, it was concluded that: (1) with growing barn owl population, the number of sequential broods increases but changes in tawny owl population size have no effect on the frequency of sequential broods; (2) the number of killings depends on the number of sequential broods; and (3) with growing barn owl population, the number of killings also grows and this change is unaffected by the size of the tawny owl population. However, no killing occurs as long as 50–60% of the nest boxes are unoccupied. There is no killing either until the percentage of nest boxes occupied by barn owls reaches 40%, although a threshold value like this cannot be shown for the tawny owl. In the cases when a barn owl breeding follows the tawny owl's, the percentage of killing is significantly higher compared to that when barn owls do not breed in the same box. These results indicate that barn owls kill the offspring of tawny owls. By these means, they obtain a breeding place earlier than without killing the chicks of the other species, and this results in higher reproductive success. © 2008 The Linnean Society of London, Biological Journal of the Linnean Society, 2008, 95 , 488–494.     

Coding of sound location and frequency in the auditory midbrain of diurnal birds of prey,families accipitridae and falconidae

Summary The coding of sound frequency and location in the avian auditory midbrain nucleus (nMLD) was examined in three diurnal raptors: the brown falcon (Falco berigora), the swamp harrier (Circus aeruginosus) and the brown goshawk (Accipiter fasciatus). Previously this nucleus has been studied with free field stimuli in only one other species, the barn owl (Tyto alba).We found some parallels between the organisation of nMLD in the diurnal raptors and that reported in the barn owl in that the central region of nMLD was tonotopically organised and contained cells that did not encode location, and the lateral region (nMLDl) contained cells which were sensitive to stimulus position. However, unlike the barn owl, which has units with circumscribed receptive fields, cells sensitive to stimulus location had large receptive fields which were restricted in azimuth but not in elevation (hemifield units). Such cells could not provide an acoustic space map in which both azimuthal and elevational dimensions were represented, but there was a tendency for units with contralateral borders to be found superficially, and those with ipsilateral borders to be found deep, in nMLDl. Hemifield units displayed receptive field properties consistent with the directional properties of the tympana in the presence of sound transmission through the interaural canal, if there is a central mechanism which is sensitive to interaural intensity differences.Abbreviations nMLD nucleus mesencephalicus lateralis pars dorsalis - SPL sound pressure level re 20 Pa - nMLDl lateral region of nMLD - ICC central nucleus of the inferior colliculus - ICX external nucleus of the inferior colliculus - IID interaural intensity difference - EI excitatory inhibitory     

Chemical composition of uropygial gland secretions of owls

The compositions of the uropygial gland secretions of the long-eared owl, eagle owl, and barn owl have been determined. The waxes of the first two owls, which are closely related, are composed of 2-alkyl-substituted fatty acids and n- or monomethyl-branched alcohols with even-numbered branching positions. In addition, some dimethyl-substituted alkanols were observed. In contrast to these waxes, the secretion of the barn owl is composed of 3-methyl- and 3,5-, 3,7-, 3,9-, 3,11-, 3,13-, and 3,15-dimethyl-branched fatty acids and n- as well as monomethyl-substituted alkanols branched at positions 2, 3, and 4. The mass spectra of esters of 2-alkyl-substituted fatty acids are discussed.     

Control of goal-directed and stimulus-driven attention in the brain

We review evidence for partially segregated networks of brain areas that carry out different attentional functions. One system, which includes parts of the intraparietal cortex and superior frontal cortex, is involved in preparing and applying goal-directed (top-down) selection for stimuli and responses. This system is also modulated by the detection of stimuli. The other system, which includes the temporoparietal cortex and inferior frontal cortex, and is largely lateralized to the right hemisphere, is not involved in top-down selection. Instead, this system is specialized for the detection of behaviourally relevant stimuli, particularly when they are salient or unexpected. This ventral frontoparietal network works as a 'circuit breaker' for the dorsal system, directing attention to salient events. Both attentional systems interact during normal vision, and both are disrupted in unilateral spatial neglect.     

Mapping time

Neuronal coding of temporal stimulus features can occur by means of delay lines. Given that neuronal activity is conducted through many parallel axons, there has to be a mechanism guaranteeing minimal temporal dispersion. We argue that plastic changes in synaptic transmission that are unspecifically propagated along presynaptic axons are a basis for the development of delay-line topologies. Furthermore, we show how two populations of afferents form a map of interaural time differences as found, for instance, in the laminar nucleus of the barn owl.     

Barn owl (Tyto alba) siblings vocally negotiate resources

Current theory proposes that nestlings beg to signal hunger level to parents honestly, or that siblings compete by escalating begging to attract the attention of parents. Although begging is assumed to be directed at parents, barn owl (Tyto alba) nestlings vocalize in the presence but also in the absence of the parents. Applying the theory of asymmetrical contests we experimentally tested three predictions of the novel hypothesis that in the absence of the parents siblings vocally settle contests over prey items to be delivered next by a parent. This 'sibling negotiation hypothesis' proposes that offspring use each others' begging vocalization as a source of information about their relative willingness to contest the next prey item delivered. In line with the hypothesis we found that (i) a nestling barn owl refrains from vocalization when a rival is more hungry, but (ii) escalates once the rival has been fed by a parent, and (iii) nestlings refrain from and escalate vocalization in experimentally enlarged and reduced broods, respectively. Thus, when parents are not at the nest a nestling vocally refrains when the value of the next delivered prey item will be higher for its nest-mates. These findings are the exact opposite of what current models predict for begging calls produced in the presence of the parents.     

The effect of predictability on subjective duration

Events can sometimes appear longer or shorter in duration than other events of equal length. For example, in a repeated presentation of auditory or visual stimuli, an unexpected object of equivalent duration appears to last longer. Illusions of duration distortion beg an important question of time representation: when durations dilate or contract, does time in general slow down or speed up during that moment? In other words, what entailments do duration distortions have with respect to other timing judgments? We here show that when a sound or visual flicker is presented in conjunction with an unexpected visual stimulus, neither the pitch of the sound nor the frequency of the flicker is affected by the apparent duration dilation. This demonstrates that subjective time in general is not slowed; instead, duration judgments can be manipulated with no concurrent impact on other temporal judgments. Like spatial vision, time perception appears to be underpinned by a collaboration of separate neural mechanisms that usually work in concert but are separable. We further show that the duration dilation of an unexpected stimulus is not enhanced by increasing its saliency, suggesting that the effect is more closely related to prediction violation than enhanced attention. Finally, duration distortions induced by violations of progressive number sequences implicate the involvement of high-level predictability, suggesting the involvement of areas higher than primary visual cortex. We suggest that duration distortions can be understood in terms of repetition suppression, in which neural responses to repeated stimuli are diminished.     

Composition of the body mass overshoot in European barn owl nestlings (Tyto alba ): insurance against scarcity of energy or water?

European barn owl chicks (Tyto alba) show a body mass overshoot prior to fledging that has been predicted to serve as an energy reservoir during periods of stochastic food availability. However, the composition of the mass overshoot has heretofore not been directly examined in nestlings of this or any other species displaying a body mass overshoot during growth (e.g., raptors and seabirds). To experimentally determine whether the overshoot in body mass in juvenile European barn owls (Tyto alba) may act as an energy reservoir, we compared the body composition of owl chicks raised on an ad libitum diet to those fed a restricted diet designed to eliminate the overshoot. Chicks raised on the two diets were also compared for differences in maturation of diverse functions (e.g., locomotion) and tissues (e.g., skeletal development). Contrary to expectations, our results on body composition in juvenile barn owls indicate that the mass overshoot prior to fledging is primarily comprised of an increased water compartment. Thus, we suggest that the mass overshoot in owls (and possibly in other species) does not serve as an energy reservoir but, rather, may function as an insurance against dehydration when hot in-nest conditions force chicks to rely on evaporative cooling: temperatures in barn owl nests can reach up to 43 degrees C. We found no significant differences in maturation indexes between diet treatments at the time of fledging.     

Effects of different sexual stimuli on oxytocin release,uterine activity and receptive behavior in estrous sows

This study was designed to assess effects of exogenous oxytocin (OT) on uterine activity, and to compare three different sexual stimuli in their effects on OT release, uterine activity and receptive behavior in estrous sows. Uterine activity was recorded nonsurgically, by transcervical insertion of an open-end catheter into the caudal part of the uterine lumen. After recording spontaneous uterine activity, exogenous OT was administered (Experiment 1), or one of the following stimuli was applied to the sow (Experiment 2): tactile stimuli, i.e. manual stimulation of the sow's back and flanks, tactile stimulation in combination with boar pheromone spray (5alpha-androstenon), or tactile stimuli in the presence of a boar. Both exogenous OT and endogenously released OT increased uterine activity. The effect depended on the uterine activity before treatment, with the effect being greater in those sows with lower uterine activity before treatment. In Experiment 2, boar presence was the only stimulus that elicited a clear, surge-like release of OT, and also clearly increased uterine activity. Release of OT was not necessary for induction of receptive behavior: tactile stimulation alone and in combination with pheromone spray elicited a standing response in one third of the sows, but had no effect on OT release.     

Coding interaural time differences at low best frequencies in the barn owl.

In birds and mammals, precisely timed spikes encode the timing of acoustic stimuli, and interaural acoustic disparities propagate to binaural processing centers. The Jeffress model proposes that these projections act as delay lines to innervate an array of coincidence detectors, every element of which has a different relative delay between its ipsilateral and contralateral excitatory inputs. Thus, interaural time difference (ITD) is encoded into the position of the coincidence detector whose delay lines best cancel out the acoustic ITD. Neurons of the avian nucleus laminaris and mammalian MSO phase-lock to both monaural and binaural stimuli but respond maximally when phase-locked spikes from each side arrive simultaneously, i.e. when the difference in the conduction delays compensates for the ITD. McAlpine et al. [Nat. Neurosci. 4 (2001) 396] identified an apparent difference between avian and mammalian ITD coding. In the barn owl, the maximum firing rate appears to encode ITD. This may not be the case for the guinea pig, where the steepest region of the function relating discharge rate to interaural time delay (ITD) is close to midline for all neurons, irrespective of best frequency (BF). These data suggest that low BF ITD sensitivity in the guinea pig is mediated by detection of a change in slope of the ITD function, and not by maximum rate. We review coding of low best frequency ITDs in barn owls and mammals and discuss whether there may be differences in the code used to signal ITD in mammals and birds.     

Abnormal distracter processing in adults with attention-deficit-hyperactivity disorder

Background

Subjects with Attention-Deficit Hyperactivity Disorder (ADHD) are overdistractible by stimuli out of the intended focus of attention. This control deficit could be due to primarily reduced attentional capacities or, e. g., to overshooting orienting to unexpected events. Here, we aimed at identifying disease-related abnormalities of novelty processing and, therefore, studied event-related potentials (ERP) to respective stimuli in adult ADHD patients compared to healthy subjects.

Methods

Fifteen unmedicated subjects with ADHD and fifteen matched controls engaged in a visual oddball task (OT) under simultaneous EEG recordings. A target stimulus, upon which a motor response was required, and non-target stimuli, which did not demand a specific reaction, were presented in random order. Target and most non-target stimuli were presented repeatedly, but some non-target stimuli occurred only once (‘novels’). These unique stimuli were either ‘relative novels’ with which a meaning could be associated, or ‘complete novels’, if no association was available.

Results

In frontal recordings, a positive component with a peak latency of some 400 ms became maximal after novels. In healthy subjects, this novelty-P3 (or ‘orienting response’) was of higher magnitude after complete than after relative novels, in contrast to the patients with an undifferentially high frontal responsivity. Instead, ADHD patients tended to smaller centro-parietal P3 responses after target signals and, on a behavioural level, responded slower than controls.

Conclusion

The results demonstrate abnormal novelty processing in adult subjects with ADHD. In controls, the ERP pattern indicates that allocation of meaning modulates the processing of new stimuli. However, in ADHD such a modulation was not prevalent. Instead, also familiar, only context-wise new stimuli were treated as complete novels. We propose that disturbed semantic processing of new stimuli resembles a mechanism for excessive orienting to commonly negligible stimuli in ADHD.     

The relationship between intra–guild diet overlap and breeding in owls in Israel

Even though intra-guild predators frequently prey on the same species, it is unclear whether diet overlap between two predators is a source of interspecific competition or whether predators simply use the same abundant prey resource. We measured the extent to which the diets of barn owls (Tyto alba) and long-eared owls (Asio otus) in Israel overlap and examined whether yearly differences in diet overlap correlate with barn owl breeding success. Pianka’s index of niche overlap was positively related to barn owl population size but not to its breeding success. The number of breeding barn owls was higher when long-eared owls consumed more rodents, suggesting that diet overlap most likely increased when rodents became more abundant. Therefore, in Israel, when these two owl species prey more often on rodents, their diets are more similar and interspecific competition is reduced. Unlike sympatric populations in Europe, in years when rodents are less abundant in Israel long-eared owls switch to hunting alternative prey (e.g., birds), perhaps to avoid competition with barn owls.