Behavioral and neuronal study of inhibition of return in barn owls.
ABSTRACT: Inhibition of return (IOR) is the reduction of detection speed and/or detection accuracy of a target in a recently attended location. This phenomenon, which has been discovered and studied thoroughly in humans, is believed to reflect a brain mechanism for controlling the allocation of spatial attention in a manner that enhances efficient search. Findings showing that IOR is robust, apparent at a very early age and seemingly dependent on midbrain activity suggest that IOR is a universal attentional mechanism in vertebrates. However, studies in non-mammalian species are scarce. To explore this hypothesis comparatively, we tested for IOR in barn owls (Tyto alba) using the classical Posner cueing paradigm. Two barn owls were trained to initiate a trial by fixating on the center of a computer screen and then turning their gaze to the location of a target. A short, non-informative cue appeared before the target, either at a location predicting the target (valid) or a location not predicting the target (invalid). In one barn owl, the response times (RT) to the valid targets compared to the invalid targets shifted from facilitation (lower RTs) to inhibition (higher RTs) when increasing the time lag between the cue and the target. The second owl mostly failed to maintain fixation and responded to the cue before the target onset. However, when including in the analysis only the trials in which the owl maintained fixation, an inhibition in the valid trials could be detected. To search for the neural correlates of IOR, we recorded multiunit responses in the optic tectum (OT) of four head-fixed owls passively viewing a cueing paradigm as in the behavioral experiments. At short cue to target lags (<100?ms), neural responses to the target in the receptive field (RF) were usually enhanced if the cue appeared earlier inside the RF (valid) and were suppressed if the cue appeared earlier outside the RF (invalid). This was reversed at longer lags: neural responses were suppressed in the valid conditions and were unaffected in the invalid conditions. The findings support the notion that IOR is a basic mechanism in the evolution of vertebrate behavior and suggest that the effect appears as a result of the interaction between lateral and forward inhibition in the tectal circuitry.
Project description:Peripheral cueing tasks can be used to measure reflexive (automatic) attention. In these tasks, increases in response time or RT (costs) typically follow contralateral (invalid) cues as attention must move from the location of the cue to the target. Reductions in RT (benefits) to a target typically follow ipsilateral (valid) cues because the cue draws attention to where the target will appear. Two exceptions to RT benefits are inhibition of return (IOR) and masking. IOR is the tendency to respond slower to targets that appear in locations attended within the last 200-2000 ms. Masking occurs when the visibility of a target is blocked by another stimulus (e.g., the cue). Herein, we describe two experiments, both using a modified Posner task with "earth rockets" as cues and "alien spaceships" as targets. Cues were equally likely to appear on the left or right side of a display following targets. Participants were instructed to press a left or right key corresponding to a left or right target. In Experiment 1, we obtained data from 203 children (10.58-16.55 years old). We discovered unexpected costs following cues that typically provide RT benefits. In Experiment 2, we explored IOR, masking, and age differences in the occurrence of these costs. We manipulated the cue-target temporal distance ("stimulus onset asynchrony" or SOA) to explore IOR and the cue-target spatial distance to explore masking. We also considered a wider age range. Sixty-three children and 41 young adults participated. Experiment 2 revealed a three-way interaction between SOA, spatial distance, and age. At the shorter SOA (100 ms) and moderate spatial distance, unexpected costs followed valid cues for younger children (7.07-10.15 years old). These costs also occurred in young adults (18.00-23.02 years old) following far distance cues at this SOA. At the longer SOA (200 ms), these costs followed moderate and far cues for younger children and near cues for young adults. Older children (10.31-14.92 years) did not have unexpected costs. We explain the findings in terms of masking, IOR, and possible developmental mechanisms.
Project description:Typical avian eyes are phenotypically engineered for photopic vision (daylight). In contrast, the highly derived eyes of the barn owl (Tyto alba) are adapted for scotopic vision (dim light). The dramatic modifications distinguishing barn owl eyes from other birds include: 1) shifts in frontal orientation to improve binocularity, 2) rod-dominated retina, and 3) enlarged corneas and lenses. Some of these features parallel mammalian eye patterns, which are hypothesized to have initially evolved in nocturnal environments. Here, we used an integrative approach combining phylogenomics and functional phenotypes of 211 eye-development genes across 48 avian genomes representing most avian orders, including the stem lineage of the scotopic-adapted barn owl. Overall, we identified 25 eye-development genes that coevolved under intensified or relaxed selection in the retina, lens, cornea, and optic nerves of the barn owl. The agtpbp1 gene, which is associated with the survival of photoreceptor populations, was pseudogenized in the barn owl genome. Our results further revealed that barn owl retinal genes responsible for the maintenance, proliferation, and differentiation of photoreceptors experienced an evolutionary relaxation. Signatures of relaxed selection were also observed in the lens and cornea morphology-associated genes, suggesting that adaptive evolution in these structures was essentially structural. Four eye-development genes (ephb1, phactr4, prph2, and rs1) evolved in positive association with the orbit convergence in birds and under relaxed selection in the barn owl lineage, likely contributing to an increased reliance on binocular vision in the barn owl. Moreover, we found evidence of coevolutionary interactions among genes that are expressed in the retina, lens, and optic nerve, suggesting synergetic adaptive events. Our study disentangles the genomic changes governing the binocularity and low-light perception adaptations of barn owls to nocturnal environments while revealing the molecular mechanisms contributing to the shift from the typical avian photopic vision to the more-novel scotopic-adapted eye.
Project description:BACKGROUND: Understanding the ecological consequences of roads and developing ways to mitigate their negative effects has become an important goal for many conservation biologists. Most mitigation measures are based on road mortality and barrier effects data. However, studying fine-scale individual spatial responses in roaded landscapes may help develop more cohesive road planning strategies for wildlife conservation. METHODOLOGY/PRINCIPAL FINDINGS: We investigated how individuals respond in their spatial behavior toward a highway and its traffic intensity by radio-tracking two common species particularly vulnerable to road mortality (barn owl Tyto alba and stone marten Martes foina). We addressed the following questions: 1) how highways affected home-range location and size in the immediate vicinity of these structures, 2) which road-related features influenced habitat selection, 3) what was the role of different road-related features on movement properties, and 4) which characteristics were associated with crossing events and road-kills. The main findings were: 1) if there was available habitat, barn owls and stone martens may not avoid highways and may even include highways within their home-ranges; 2) both species avoided using areas near the highway when traffic was high, but tended to move toward the highway when streams were in close proximity and where verges offered suitable habitat; and 3) barn owls tended to cross above-grade highway sections while stone martens tended to avoid crossing at leveled highway sections. CONCLUSIONS: Mortality may be the main road-mediated mechanism that affects barn owl and stone marten populations. Fine-scale movements strongly indicated that a decrease in road mortality risk can be realized by reducing sources of attraction, and by increasing road permeability through measures that promote safe crossings.
Project description:The three subspecies of Spotted Owl (Northern, Strix occidentalis caurina; California, S. o. occidentalis; and Mexican, S. o. lucida) are all threatened by habitat loss and range expansion of the Barred Owl (S. varia). An unaddressed threat is whether Barred Owls could be a source of novel strains of disease such as avian malaria (Plasmodium spp.) or other blood parasites potentially harmful for Spotted Owls. Although Barred Owls commonly harbor Plasmodium infections, these parasites have not been documented in the Spotted Owl. We screened 111 Spotted Owls, 44 Barred Owls, and 387 owls of nine other species for haemosporidian parasites (Leucocytozoon, Plasmodium, and Haemoproteus spp.). California Spotted Owls had the greatest number of simultaneous multi-species infections (44%). Additionally, sequencing results revealed that the Northern and California Spotted Owl subspecies together had the highest number of Leucocytozoon parasite lineages (n = 17) and unique lineages (n = 12). This high level of sequence diversity is significant because only one Leucocytozoon species (L. danilewskyi) has been accepted as valid among all owls, suggesting that L. danilewskyi is a cryptic species. Furthermore, a Plasmodium parasite was documented in a Northern Spotted Owl for the first time. West Coast Barred Owls had a lower prevalence of infection (15%) when compared to sympatric Spotted Owls (S. o. caurina 52%, S. o. occidentalis 79%) and Barred Owls from the historic range (61%). Consequently, Barred Owls on the West Coast may have a competitive advantage over the potentially immune compromised Spotted Owls.
Project description:Gaze direction is an important social communication tool. Global and local visual information are known to play specific roles in processing socially relevant information from a face. The current study investigated whether global visual information has a primary role during gaze-cued orienting of attention and, as such, may influence quality of interaction. Adults performed a gaze-cueing task in which a centrally presented face cued (valid or invalid) the location of a peripheral target through a gaze shift. We measured brain activity (electroencephalography) towards the cue and target and behavioral responses (manual and saccadic reaction times) towards the target. The faces contained global (i.e. lower spatial frequencies), local (i.e. higher spatial frequencies), or a selection of both global and local (i.e. mid-band spatial frequencies) visual information. We found a gaze cue-validity effect (i.e. valid versus invalid), but no interaction effects with spatial frequency content. Furthermore, behavioral responses towards the target were in all cue conditions slower when lower spatial frequencies were not present in the gaze cue. These results suggest that whereas gaze-cued orienting of attention can be driven by both global and local visual information, global visual information determines the speed of behavioral responses towards other entities appearing in the surrounding of gaze cue stimuli.
Project description:Reorienting of voluntary attention enables the processing of stimuli at previously unattended locations. Although studies have identified a ventral fronto-parietal network underlying attention [1, 2], little is known about whether and how early visual areas are involved in involuntary [3, 4] and even less in voluntary  reorienting, and their temporal dynamics are unknown. We used transcranial magnetic stimulation (TMS) over the occipital cortex to interfere with attentional reorienting and study its role and temporal dynamics in this process. Human observers performed an orientation discrimination task, with either valid or invalid attention cueing, across a range of stimulus contrasts. Valid cueing induced a behavioral response gain increase, higher asymptotic performance for attended than unattended locations. During subsequent TMS sessions, observers performed the same task, with high stimulus contrast. Based on phosphene mapping, TMS double pulses were applied at one of various delays to a consistent brain location in retinotopic areas (V1/V2), corresponding to the evoked signal of the target or distractor, in a valid or invalid trial. Thus, the stimulation was identical for the four experimental conditions (valid/invalid cue condition × target/distractor-stimulated). TMS modulation of the target and distractor were both periodic (5 Hz, theta) and out of phase with respect to each other in invalid trials only, when attention had to be disengaged from the distractor and reoriented to the target location. Reorientation of voluntary attention periodically involves V1/V2 at the theta frequency. These results suggest that TMS probes theta phase-reset by attentional reorienting and help link periodic sampling in time and attention reorienting in space.
Project description:We measured the auditory sensitivity of the barn owl (Tyto alba), using a behavioural Go/NoGo paradigm in two different age groups, one younger than 2 years (n = 4) and another more than 13 years of age (n = 3). In addition, we obtained thresholds from one individual aged 23 years, three times during its lifetime. For computing audiograms, we presented test frequencies of between 0.5 and 12 kHz, covering the hearing range of the barn owl. Average thresholds in quiet were below 0 dB sound pressure level (SPL) for frequencies between 1 and 10 kHz. The lowest mean threshold was -12.6 dB SPL at 8 kHz. Thresholds were the highest at 12 kHz, with a mean of 31.7 dB SPL. Test frequency had a significant effect on auditory threshold but age group had no significant effect. There was no significant interaction between age group and test frequency. Repeated threshold estimates over 21 years from a single individual showed only a slight increase in thresholds. We discuss the auditory sensitivity of barn owls with respect to other species and suggest that birds, which generally show a remarkable capacity for regeneration of hair cells in the basilar papilla, are naturally protected from presbycusis.
Project description:BACKGROUND: Owls possess an extraordinary neck and head mobility. To understand this mobility it is necessary to have an anatomical description of cervical vertebrae with an emphasis on those criteria that are relevant for head positioning. No functional description specific to owls is available. METHODOLOGY/PRINCIPAL FINDINGS: X-ray films and micro-CT scans were recorded from American barn owls (Tyto furcata pratincola) and used to obtain three-dimensional head movements and three-dimensional models of the 14 cervical vertebrae (C1-C14). The diameter of the vertebral canal, the zygapophyseal protrusion, the distance between joint centers, and the pitching angle were quantified. Whereas the first two variables are purely osteological characteristics of single vertebrae, the latter two take into account interactions between vertebrae. These variables change in characteristic ways from cranial to caudal. The vertebral canal is wide in the cranial and caudal neck regions, but narrow in the middle, where both the zygapophyseal protrusion and the distance between joint centers are large. Pitching angles are more negative in the cranial and caudal neck regions than in the middle region. Cluster analysis suggested a complex regionalization. Whereas the borders (C1 and C13/C14) formed stable clusters, the other cervical vertebrae were sorted into 4 or 5 additional clusters. The borders of the clusters were influenced by the variables analyzed. CONCLUSIONS/SIGNIFICANCE: A statistical analysis was used to evaluate the regionalization of the cervical spine in the barn owl. While earlier measurements have shown that there appear to be three regions of flexibility of the neck, our indicators suggest 3-7 regions. These many regions allow a high degree of flexibility, potentially facilitating the large head turns that barn owls are able to make. The cervical vertebral series of other species should also be investigated using statistical criteria to further characterize morphology and the potential movements associated with it.
Project description:Previous studies have shown that emotional facial expressions capture visual attention. However, it has been unclear whether attentional modulation is attributable to their emotional significance or to their visual features. We investigated this issue using a spatial cueing paradigm in which non-predictive cues were peripherally presented before the target was presented in either the same (valid trial) or the opposite (invalid trial) location. The target was an open dot and the cues were photographs of normal emotional facial expressions of anger and happiness, their anti-expressions and neutral expressions. Anti-expressions contained the amount of visual changes equivalent to normal emotional expressions compared with neutral expressions, but they were usually perceived as emotionally neutral. The participants were asked to localize the target as soon as possible. After the cueing task, they evaluated their subjective emotional experiences to the cue stimuli. Compared with anti-expressions, the normal emotional expressions decreased and increased the reaction times (RTs) in the valid and invalid trials, respectively. Shorter RTs in the valid trials and longer RTs in the invalid trials were related to higher subjective arousal ratings. These results suggest that emotional facial expressions accelerate attentional engagement and prolong attentional disengagement due to their emotional significance.
Project description:Faces that consistently shifted the gaze to subsequent target locations in a gaze cueing task were chosen as being more trustworthy than faces that always looked away from the target, suggesting that the validity of a gaze cue influenced the viewers' judgments regarding the trustworthiness of human faces. We investigated whether the gaze cueing effect and judgments regarding the personality conveyed by a face would be affected by the valence of a target. A face image moved its eyes to the left or the right, and an emotional target image (positive, negative, or neutral) appeared to left or right of the face. Participants had to indicate the location of this target by pressing a key. The target image was preceded by a face that shifted its gaze to the target image (valid cue), a face that directed its gaze to the opposite side (invalid cue), or a face that did not move its eyes (no cue). The perceived trustworthiness of the face was evaluated after the gaze-cueing task. Results showed that faces that looked at positive targets were evaluated as more trustworthy than faces that looked at negative targets. However, the valence of the targets did not affect trustworthiness ratings in invalid and no-cue conditions. We suggest that integrated information about the predictability of the gaze cue and the valence of the gaze target modulates impressions about the personality of the face.