Neural representations of space in the hippocampus of a food-caching bird

Abstract

Spatial memory in vertebrates requires brain regions homologous to the mammalian hippocampus. Between vertebrate clades, however, these regions are anatomically distinct and appear to produce different spatial patterns of neural activity. We asked whether hippocampal activity is fundamentally different even between distant vertebrates that share a strong dependence on spatial memory. We studied tufted titmice, food-caching birds capable of remembering many concealed food locations. We found mammalian-like neural activity in the titmouse hippocampus, including sharp-wave ripples and anatomically organized place cells. In a non–food-caching bird species, spatial firing was less informative and was exhibited by fewer neurons. These findings suggest that hippocampal circuit mechanisms are similar between birds and mammals, but that the resulting patterns of activity may vary quantitatively with species-specific ethological needs.

Active exploration of a novel environment drives the activation of the hippocampus-amygdala complex of domestic chicks

“…To best of our knowledge, so far only two other studies investigated the involvement of the avian hippocampus in the exploration of novel environments (Mayer et al, 2018;Morandi-Raikova and Mayer, 2020). Altogether, these studies contribute to the vast literature showing that, despite the fundamental differences in the structure of the hippocampal formation in birds and mammals (Striedter, 2016), its involvement in spatial 14 functions is shared among the two clades (Bingman et al, 2005;Siegel et al, 2005;Hough and Bingman, 2008;Kahn and Bingman, 2009;Mayer et al, 2010Mayer et al, , 2013Mayer et al, , 2016Mayer and Bischof, 2013;Coppola et al, 2015Coppola et al, , 2016Sherry et al, 2017;Lormat et al, 2020;Morandi-Raikova and Mayer, 2021;Payne et al, 2021).…”

“…The more locations are visited the higher number of hippocampal cells should express c-Fos. Moreover, based on previous studies carried out in other bird species, one can expect to find a higher degree of activation in the anterior segment of Hp during spatial mapping (Payne et al, 2021). However, no study so far reported differences in activation between the anterior, intermediate, and posterior hippocampal segments in domestic chicks.…”

“…We expected to find more c-Fos immunoreactive cells after active exploration of the novel environment. Moreover, we expected that this increased activity would be more visible in the anterior segment of chicks' hippocampus, as observed in titmice, zebra finches, and owls (Agarwal et al, 2021 preprint;Payne et al, 2021). We also measured the activation of nucleus taeniae of amygdala (TnA), which is a homolog of the mammalian medial amygdala (Abelan et al, 2009).…”

“…However, at present it is not clear if this activation/plasticity of the hippocampus is induced by the mere visual input from the novel environment or if it requires active exploration of the environment. If hippocampal IEGs expression is related to the activation of spatially responsive cells (place cells, boundary cells etc., Ben-Yishay et al, 2021;Payne at al., 2021), active exploration of a novel environment should cause a higher number of c-Fos expressing cells. Whenever a new location is visited during the exploration, the cells that encode the corresponding location should increase their firing rate, inducing c-Fos expression.…”

“…In birds too, hippocampal place cells (Payne et al, 2021) and head direction cells (Ben-Yishay et al, 2021; Takahashi et al, 2022) have been recently found. Payne et al, (2021) found place cells in two different species of birds: tufted titmice ( Baeolophus bicolor ) and zebra finches ( Taeniopygia guttata ). Interestingly, the spatially responsive cells observed in these two bird species were located predominantly in the anterior hippocampus.…”