One important aspect of my ERC-project is the analysis of the avian hippocampus and its putative memory function. To this end, we conducted a detailed anatomical analysis of the intrahippocampal connectivity patterns in pigeons (Rook et al., 2023). Our techniques revealed a complex connectivity pattern along the hippocampal transverse axis that started in the dorsolateral hippocampus and continued to the dorsomedial subdivision, from where information was relayed to the triangular region either directly or indirectly via the V-shaped layers. The often-reciprocal connectivity along these subdivisions displayed an intriguing topographical arrangement such that two parallel pathways could be discerned along the ventrolateral (deep) and dorsomedial (superficial) aspects of the avian hippocampus. Overall, our findings provide an unprecedented, detailed description of avian intrahippocampal pathway and provide further support for the hypothesized homology of the lateral V-shape layer and the dorsomedial hippocampus with the dentate gyrus and Ammon’s horn of mammals, respectively.
A core technique of the project is fMRI in awake birds under ultrahigh magnetic fieldconditions. However, this is challenging due to strong local magnetic field inhomogeneities caused by air cavities in the avian skull. Therefore, we developed a two-segmented spin-echo echo-planar imaging (SE-EPI) sequence that covers the whole brain of awake pigeons. This sequence was applied to investigate sensory networks in awake pigeons and assessed the relative merits of this method in comparison with the classic single-shot RARE sequence. At the same imaging resolution but with a volume acquisition of 3 s versus 4 s for RARE, the two-segmented SE-EPI provided twice the strength of BOLD activity compared with the single-shot RARE sequence, while the image signal-to-noise ratio (SNR) and in particular the temporal SNR were very similar for the two sequences. In addition, the activation patterns in two-segmented SE-EPI data were more symmetric and larger than single-shot RARE results. Two-segmented SE-EPI thus represents a valid alternative to the RARE sequence in avian fMRI research since it yields more than twice the BOLD sensitivity per unit of time with much less energy deposition and better temporal resolution, particularly for event-related experiments. This will greatly benefit the project (Khodadadi et al., 2023).
One of our hypotheses was that the constitution of memory engrams go along with an activation of the avian hippocampus (or other structures). To this end, we studied filial imprinting in chicks by developing a ground-breaking non-invasive functional MRI technique for awake, newly hatched chicks that record whole-brain BOLD signal changes throughout imprinting experiments. Our findings identified potential long-term storage areas of imprinting memories across a neural network that included the hippocampal formation, providing strong support for its memory function in birds (Behroozi et al., in revision).
A key aim of this ERC was to identify cognitive networks. As a first approach, we studied dream patterns in pigeons within an ultrahigh magnetic force fMRI system. We show that REM sleep, a paradoxical state with wake-like brain activity, during which we experience our most vivid dreams, is accompanied in birds with the activation of networks involved in processing visual information, including optic flow during flight (Ungurean et al., 2023).
One of the aims of my ERC is to show consciousness in avian species that is not regarded as “feathered apes” like corvids. Many scientists ascribe the ability to recognize oneself in the mirror as a correlate of consciousness. Up to now, this ability was only shown in a few corvid species. We now used a completely novel approach by using roosters (which do not pass the usual mark-and-mirror test) under ecologically appropriate conditions: Roosters warn conspecifics when seeing an aerial predator, but not when alone. Exploiting this natural behavior, we tested individual roosters alone, with another male, or with a mirror while a hawk’s silhouette flew above them. Roosters mainly emitted alarm calls in the presence of another individual but not when alone or seeing themselves in the mirror. Thus, chickens possibly recognize their reflection as their own but only when tested under a condition in which they differentiate between alone or being accompanied by other chicken. This study shows how strikingly strong cognition is ecologically embedded (Hillemacher et al., 2023).
Using a similar ecological approach, we analyzed in greatest detail pigeons’ decision processes when being confronted with various options during a semi-natural foraging task. Our results indicate that hungry pigeons preferred to peck for delay reduction but did not work more for that option than for probability increase, which was the most profitable alternative and did not induce more pecking effort. These results cast a new light on current foraging theories and make it likely that avian decisions integrate many economic variables (Wittek et al., 2024).
In a major review (Güntürkün et al., 2024), we then outlined first pillars of a new theory why birds are smart. We propose four features that may be required for complex cognition: first, many associative pallial neurons, second, a prefrontal cortex (PFC)-like area, third, a dense dopaminergic innervation of association areas that feedback the outcome of own decisions, and fourth, dynamic neurophysiological fundaments withing the beta- and gamma-range for working memory. These four neural features have convergently evolved and may therefore represent ‘hard to replace’ mechanisms enabling complex cognition. Importantly, we could show that seemingly simple computational models can show that some of these properties, like large numbers of associative pallial neurons, rest on the power of associative learning—a process that is often underestimated in cognitive science (Wasserman et al., 2024).
