Neural evidence for referential understanding of object words in dogs.

Using words to refer to objects in the environment is a core feature of the human language faculty. Referential understanding assumes the formation of mental representations of these words.1,2 Such understanding of object words has not yet been demonstrated as a general capacity in any non-human species,3 despite multiple behavior-based case reports.4,5,6,7,8,9,10 In human event-related potential (ERP) studies, object word knowledge is typically tested using the semantic violation paradigm, where words are presented either with their referent (match) or another object (mismatch).11,12 Such mismatch elicits an N400 effect, a well-established neural correlate of semantic processing.12,13 Reports of preverbal infant N400 evoked by semantic violations14 assert the use of this paradigm to probe mental representations of object words in nonverbal populations. Here, measuring dogs' (Canis familiaris) ERPs to objects primed with matching or mismatching object words, we found a mismatch effect at a frontal electrode, with a latency (206-606 ms) comparable to the human N400. A greater difference for words that dogs knew better, according to owner reports, further supported a semantic interpretation of this effect. Semantic expectations emerged irrespective of vocabulary size, demonstrating the prevalence of referential understanding in dogs. These results provide the first neural evidence for object word knowledge in a non-human animal. VIDEO ABSTRACT.

Out-of-reach rewards elicit human-oriented referential communicative behaviours in family dogs but not in family pigs.

Human-oriented referential communication has been evidenced not only in domestic but also in some wild species, however, the importance of domestication-unrelated species' characteristics in the emergence of this capacity remains largely unexplored. One shared property of all species reported to exhibit referential communication is the efficient use of visual social signals. To assess the potential role of species-specific characteristics in the emergence of human-oriented referential communication, we compared similarly socialised companion animals from two domestic species: dogs, which rely heavily on conspecific visual social signals; and pigs, which do not. We used an out-of-reach reward paradigm with three conditions: both human and reward present, only human present, only reward present. Both species exhibited certain behaviours (e.g. orientation towards the human, orientation alternation between the human and the reward) more often in the human's presence. However, only dogs exhibited those behaviours more often in the simultaneous presence of the human and the reward. These results suggest similar readiness in dogs and pigs to attend to humans but also that pigs, unlike dogs, do not initiate referential communication with humans. The ability to referentially communicate with humans may not emerge in mammals, even if domesticated companion animals, that lack certain species characteristics, such as efficient intraspecific visual communication.

Transcriptomics of Parental Care in the Hypothalamic-Septal Region of Female Zebra Finch Brain.

(1) Background: The objective of this study was to uncover genomic causes of parental care. Since birds do not lactate and, therefore, do not show the gene expressional changes required for lactation, we investigate gene expression associated with parenting in caring and non-caring females in an avian species, the small passerine bird zebra finch (Taeniopygia guttata). Here, we compare expression patterns in the hypothalamic-septal region since, previously, we showed that this area is activated in parenting females. (2) Methods: Transcriptome sequencing was first applied in a dissected part of the zebra finch brain related to taking care of the nestlings as compared to a control group of social pairs without nestlings. (3) Results: We found genes differentially expressed between caring and non-caring females. When introducing a log2fold change threshold of 1.5, 13 annotated genes were significantly upregulated in breeding pairs, while 39 annotated genes were downregulated. Significant enrichments of dopamine and acetylcholine biosynthetic processes were identified among upregulated pathways, while pro-opiomelanocortin and thyroid hormone pathways were downregulated, suggesting the importance of these systems in parental care. Network analysis further suggested neuro-immunological changes in mothers. (4) Conclusions: The results confirm the roles of several hypothesized major pathways in parental care, whereas novel pathways are also proposed.

Neuronal activation in zebra finch parents associated with reintroduction of nestlings.

Recent studies of the brain mechanisms of parental behaviors have mainly focused on rodents. Using other vertebrate taxa, such as birds, can contribute to a more comprehensive, evolutionary view. In the present study, we investigated a passerine songbird, the zebra finch (Taeniopygia guttata), with a biparental caring system. Parenting-related neuronal activation was induced by first temporarily removing the nestlings, and then, either reuniting the focal male or female parent with the nestlings (parental group) or not (control group). To identify activated neurons, the immediate early gene product, Fos protein, was labeled. Both parents showed an increased level of parental behavior following reunion with the nestlings, and no sexual dimorphism occurred in the neuronal activation pattern. Offspring-induced parental behavior-related neuronal activation was found in the preoptic, ventromedial (VMH), paraventricular hypothalamic nuclei, and in the bed nucleus of the stria terminalis. In addition, the number of Fos-immunoreactive (Fos-ir) neurons in the nucleus accumbens predicted the frequency of the feeding of the nestlings. No difference was found in Fos expression when the effect of isolation or the presence of the mate was examined. Thus, our study identified a number of nuclei involved in parental care in birds and suggests similar regulatory mechanisms in caring females and males. The activated brain regions show similarities to rodents, while a generally lower number of brain regions were activated in the zebra finch. Furthermore, future studies are necessary to establish the role of the apparently avian-specific neuronal activation in the VMH of zebra finch parents.

Diurnal and Reproductive Stage-Dependent Variation of Parental Behaviour in Captive Zebra Finches.

Parental care plays a key role in ontogeny, life-history trade-offs, sexual selection and intra-familial conflict. Studies focusing on understanding causes and consequences of variation in parental effort need to quantify parental behaviour accurately. The applied methods are, however, diverse even for a given species and type of parental effort, and rarely validated for accuracy. Here we focus on variability of parental behaviour from a methodological perspective to investigate the effect of different samplings on various estimates of parental effort. We used nest box cameras in a captive breeding population of zebra finches, Taeniopygia guttata, a widely used model system of sexual selection, intra-familial dynamics and parental care. We investigated diurnal and reproductive stage-dependent variation in parental effort (including incubation, brooding, nest attendance and number of feedings) based on 12h and 3h continuous video-recordings taken at various reproductive stages. We then investigated whether shorter (1h) sampling periods provided comparable estimates of overall parental effort and division of labour to those of longer (3h) sampling periods. Our study confirmed female-biased division of labour during incubation, and showed that the difference between female and male effort diminishes with advancing reproductive stage. We found individually consistent parental behaviours within given days of incubation and nestling provisioning. Furthermore, parental behaviour was consistent over the different stages of incubation, however, only female brooding was consistent over nestling provisioning. Parental effort during incubation did not predict parental effort during nestling provisioning. Our analyses revealed that 1h sampling may be influenced heavily by stochastic and diurnal variation. We suggest using a single longer sampling period (3h) may provide a consistent and accurate estimate for overall parental effort during incubation in zebra finches. Due to the large within-individual variation, we suggest repeated longer sampling over the reproductive stage may be necessary for accurate estimates of parental effort post-hatching.