Martina Manns

Cerebral lateralisation is a core organising principle of the brain that is characterised by a complex pattern of hemispheric specialisations and interhemispheric interactions. In various mental disorders, functional and/or structural hemispheric asymmetries are changed compared to healthy controls, and these alterations may contribute to the primary symptoms and cognitive impairments of a specific disorder. Since multiple genetic and epigenetic factors influence both the pathogenesis of mental illness and the development of brain asymmetries, it is likely that the neural developmental pathways overlap or are even causally intertwined, although the timing, magnitude, and direction of interactions may vary depending on the specific disorder. However, the underlying developmental steps and neuronal mechanisms are still unclear. In this review article, we briefly summarise what we know about structural, functional, and developmental relationships and outline hypothetical connections, which could be investigated in appropriate animal models. Altered cerebral asymmetries may causally contribute to the development of the structural and/or functional features of a disorder, as neural mechanisms that trigger neuropathogenesis are embedded in the asymmetrical organisation of the developing brain. Therefore, the occurrence and severity of impairments in neural processing and cognition probably cannot be understood independently of the development of the lateralised organisation of intra- and interhemispheric neuronal networks. Conversely, impaired cellular processes can also hinder favourable asymmetry development and lead to cognitive deficits in particular.

The dominance of one hemisphere for cognitive operations and decision making may be an efficient mechanism solving interhemispheric conflicts. To understand the ecological significance of the so-called metacontrol, we need better knowledge of its frequency and ontogenetic foundations. Since in pigeons, embryonic light experiences influence degree and direction of interhemispheric specialization and communication, it is conceivable that light affects metacontrol mechanisms. We therefore trained pigeons (Columba livia) with and without embryonic light stimulation in a colour discrimination task. Each eye/hemisphere learnt a different set of colours. After training, hemispheric-specific information was put into conflict and the analysis of conflict decision pattern allowed the identification of hemispheric dominance under binocular and monocular viewing conditions. A majority of pigeons displayed individual metacontrol independent of embryonic light experiences though not in the first test session. Reaction times indicate that interhemispheric mechanisms are critically involved in mediating the dominance of one hemisphere. The impact of interhemispheric components rises with increasing experience and even affects decision making under monocular seeing conditions. Overall results indicate that the hemispheres do not evaluate information independently and that interhemispheric communication in the pigeon brain is much stronger than previously thought and becomes more important with increasing experience.

Asymmetries in the functional and structural organization of the nervous system are widespread in the animal kingdom and especially characterize the human brain. Although there is little doubt that asymmetries arise through genetic and nongenetic factors, an overarching model to explain the development of functional lateralization patterns is still lacking. Current genetic psychology collects data on genes relevant to brain lateralizations, while animal research provides information on the cellular mechanisms mediating the effects of not only genetic but also environmental factors. This review combines data from human and animal research (especially on birds) and outlines a multi-level model for asymmetry formation. The relative impact of genetic and nongenetic factors varies between different developmental phases and neuronal structures. The basic lateralized organization of a brain is already established through genetically controlled embryonic events. During ongoing development, hemispheric specialization increases for specific functions and subsystems interact to shape the final functional organization of a brain. In particular, these developmental steps are influenced by environmental experiences, which regulate the fine-tuning of neural networks via processes that are referred to as ontogenetic plasticity. The plastic potential of the nervous system could be decisive for the evolutionary success of lateralized brains.

In situations where the left and right brain sides receive conflicting information that leads to incompatible response options, the brain requires efficient problem-solving mechanisms. This problem is particularly significant in lateralized brains, in which the hemispheres differ in encoding strategies or attention focus and hence, consider different information for decision-making. Meta-control, in which one hemisphere dominates ambiguous decisions, can be a mechanism that ensures fast behavioral reactions. We therefore confronted pigeons with a task in which two stimulus classes were brought into conflict. To this end, we trained pigeons simultaneously on two categories (cats or dogs) whereby each hemisphere learnt only one of the categories respectively. After learning, the birds were confronted with stimulus pairs that combined a picture with a cat (positive for one hemisphere) and a picture with a dog (positive for the other hemisphere). Pecking responses indicated the hemisphere dominating response selection. Pigeons displayed individual meta-control despite equal categorization performances of both brain hemispheres. This means that hemispheric dominance only emerged in interhemispheric conflict situations. The analysis of response latencies indicate that conflict decisions relied on intrahemispheric processes. Interhemispheric components played a role for more complex decisions. This flexibility could be a crucial building block for the evolutionary success of a lateralized brain.

In my comment on the target article of Ocklenburg et al. [Laterality 2020: Entering the next decade. Laterality, 1–33. doi:10.1080/1357650X.2020.1804396], I point out the relevance of studies in non-human species within natural settings for understanding the ecological pressures, which shape the direction and degree of brain asymmetries. I therefore outline some major research projects, which are not included in the paper of Ocklenburg et al. and which require comparative animal research.