Avian Hippocampus Spatial cognition

 

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Front Psychol. 2022 Sep 23;13:1005726. doi: 10.3389/fpsyg.2022.1005726

Spatial cognition and the avian hippocampus: Research in domestic chicks

Anastasia Morandi-Raikova 1, Uwe Mayer 1,*

Introduction

Domestic chickens are ground-living animals. Thanks to their precocial development young chicks provided an important developmental model for the study of many cognitive functions (Rosa-Salva et al., 2021). 

Chicks have been also widely used for the study of spatial orientation, complementing the research on spatial cognition in other birds, which almost exclusively used adult animals. 

Chicks can locate a goal using local cues as a beacon (Regolin et al., 1995), egocentric information (Vallortigara, 1996), distances (Vallortigara and Zanforlin, 1986; Chiesa et al., 2006), and topographical features of the environment (Rashid and Andrew, 1989). 

They can orient in relation to free-standing objects (Morandi-Raikova et al., 2020) and find the center of a square-shaped enclosure in relation to the walls (Tommasi et al., 1997; Tommasi and Vallortigara, 2000). 

Chicks can use view matching strategies (“snap-shot memories”) of the visual scenes for navigation (Dawkins and Woodington, 2000; Pecchia and Vallortigara, 2010a; Pecchia et al., 2011; but see Lee et al., 2012) and can also orient by the shape (“geometry”) of a rectangular enclosure (Vallortigara et al., 1990; Chiandetti et al., 2007, 2015; Mayer et al., 2016). In a small scale geometrical orientation task, they can use both the extended surfaces of a rectangular enclosure and a rectangular array of discrete objects (Pecchia and Vallortigara, 2010b, 2012).

Based on behavioral evidence, inferences have been often made on the involvement of chicks’ hippocampus for navigation. However, until recently, only one study directly investigated the role of chicks’ hippocampus in spatial tasks (Tommasi et al., 2003). 

We have thus performed a series of experiments using neural activity markers (the immediate early gene product c-Fos) to systematically investigate the involvement of chick hippocampus in different spatial tasks (Mayer et al., 2016, 2018; Morandi-Raikova and Mayer, 2020, 2021, 2022).

 Immediate early genes are expressed in response to neural activation and their products are often used to map neural activation in mammals and in birds (Lanahan and Worley, 1998; 

Tischmeyer and Grimm, 1999; Smulders and DeVoogd, 2000; Kubik et al., 2007; Golüke et al., 2019; Corrales Parada et al., 2021). Overall, our studies showed remarkable functional similarities in spatial processing between chicks’ hippocampus compared to adults of other bird species and to mammals. 

In this paper, we will provide a brief overview of the current state of knowledge on the hippocampal structure in birds.

 We will then present an overview of the studies that directly investigated the involvement of chicks’ hippocampus in spatial orientation, hippocampal lateralization of spatial functions and the neural mechanisms behind the encoding of locations in chicks and other birds.

Do chicks have a hippocampus?

Although this issue was debated for a long time, it is now widely accepted that the mammalian and the avian hippocampus are homologous structures (Striedter, 2015). The position and anatomical structure of

 hippocampus varies across and within different taxonomic groups. For instance, the hippocampus of rodents lies within caudal pole of the telencephalon.

 In primates, however, the hippocampus lies deep within the medial temporal lobe. 

This “dislocation” within different mammalian species was probably caused by the expansion of the cortex during evolution. Indeed, ontogenetically the mammalian hippocampus develops in the telencephalon’s dorsomedial sector and remains at that location in both marsupials and monotremes, the two “most primitive” mammalian lineages (Hevner, 2016). This is where subsequent research located the hippocampus in all sauropsids (sphenodon, lizards, snakes, turtles, crocodilians, and birds), amphibians, and cartilaginous fishes. For birds, based on topological and functional comparisons, it has been further suggested that the organization of the avian hippocampus along the anterior–posterior axis might be equivalent to the organization along the dorsoventral axis in mammalian hippocampus (Smulders, 2017; Payne et al., 2021, see Figures 1M,N). Among vertebrates, the only exception is the ray-finned fishes (actinopterygians). Due to divergent neural development, their hippocampal homolog occupies the dorsolateral telencephalon (Rodríguez et al., 2006; Moreno and González, 2007; Mueller and Wullimann, 2009). The connections of the avian hippocampus to brain areas like septum, hypothalamus, brainstem nuclei, and sensory processing areas are also similar to those found in other vertebrates, but not fully identical (Casini et al., 1986; Atoji and Wild, 2006; Striedter, 2015).