Brain morphology correlates of learning and cognitive flexibility in a fish species (Poecilia reticulata)

Abstract

Determining how variation in brain morphology affects cognitive abilities is important to understand inter-individual variation in cognition and, ultimately, cognitive evolution. Yet, despite many decades of research in this area, there is surprisingly little experimental data available from assays that quantify cognitive abilities and brain morphology in the same individuals. Here, we tested female guppies (Poecilia reticulata) in two tasks, colour discrimination and reversal learning, to evaluate their learning abilities and cognitive flexibility. We then estimated the size of five brain regions: telencephalon, optic tectum, hypothalamus, cerebellum, and dorsal medulla, in addition to relative brain size. We found that optic tectum relative size, in relation to the whole brain, correlated positively with discrimination learning performance, while relative telencephalon size correlated positively with reversal learning performance. The other brain measures were not associated with performance in either task. By evaluating how fast learning occurs and how fast an animal adjusts its learning-rules to changing conditions, we find support for that different brain regions have distinct functional correlations at the individual level. Importantly, telencephalon size emerges as an important neural correlate of higher executive functions such as cognitive flexibility. This is rare evidence supporting that more neural tissue in key brain regions confers cognitive benefits.

Executive functions and brain morphology of male and female dominant and subordinate cichlid fish

“…Although evidence suggests that enlarged brains facilitate cognitive flexibility across different species (Deaner et al 2007;Buechel et al 2018), little is known about how specific brain region sizes are associated with performance. Based on the limited research available from guppies, large telencephalons often facilitate individual performance in this task (Triki et al 2022b(Triki et al , 2023b. Our study suggests that brain regions other than the telencephalon might also play a significant role in cognitive flexibility.…”

“…During the test per se, we presented the fish with the cylinder with a food reward placed inside it. The food was placed on top of a green spot to eventually increase the salience of the food reward (Triki et al 2023b, a). To reach the reward, the fish had to detour the cylinder and swim inside.…”

“…Individuals with low inhibitory self-control abilities tend to swim straight toward the visible food and hence get blocked by the barrier. In contrast, the ability to delay gratification by moving away from the visible goal and going around the see-through barrier without touching it to reach the food reward qualifies as a high inhibitory control ability (MacLean et al 2014;Lucon-Xiccato et al 2017;Triki and Bshary 2021;Triki et al 2022aTriki et al , 2023b. Finally, the third executive function test was an object permanence task (Goulet et al 1994;Fiset et al 2003;Lowe et al 2009;Barkley 2012).…”

Experimental mosaic brain evolution improves main executive function abilities in the guppy

“…Interestingly, we detect no differences in our non-executive function assay, the colour discrimination learning. This might be because this task does not acquire complex processing but rather basic association formation through operant conditioning 53 . This is consistent with findings from fish with the entire telencephalon being removed successfully performing simple associative learning tasks 54 , while they failed in more complex tasks like reversal learning 55 .…”

“…We used survival analyses with the Cox proportional hazards models to evaluate learning performance in the colour discrimination and reversal learning tests (coxph function from R package survival). For this, we replaced "death" in the classic survival analyses with "success" in the learning tests 53 . These types of Coxph models simultaneously test both the rate of success and failure and the time to succeed.…”