A biphasic memory curve in the chambered nautilus,Nautilus pompiliusL. (Cephalopoda: Nautiloidea)

Abstract

SUMMARYCephalopods are an exceptional taxon for examining the competing influences of ecology and evolutionary history on brain and behaviour. Coleoid cephalopods (octopuses, cuttlefishes and squids) have evolved specialised brains containing dedicated learning and memory centres, and rely on plastic behaviours to hunt prey effectively and communicate intricate visual displays. Their closest living relative, the primitive nautilus, is the sole remnant of an ancient lineage that has persisted since the Cambrian. Nautilus brains are the simplest among the extant cephalopods, and the absence of dedicated learning and memory regions may represent an ancestral condition. It is assumed that the absence of these regions should limit memory storage and recall in nautilus, but this assumption has never been tested. Here we describe the first evidence of learning and memory in chambered nautilus (Nautilus pompilius). Using a Pavlovian conditioning paradigm, we demonstrate that chambered nautilus exhibits temporally separated short-and long-term memory stores, producing a characteristic biphasic memory curve similar to that of cuttlefishes. Short-term memory persisted for less than 1·h post-training, whereas long-term memory was expressed between 6 and 24·h after training. Despite lacking the dedicated neural regions that support learning and memory in all other extant cephalopods, nautilus expressed a similar memory profile to coleoids. Thus the absence of these regions in the nautilus brain does not appear to limit memory expression, as hypothesised. Our results provide valuable insights into the evolution of neural structures supporting memory.

Is behavioural flexibility evidence of cognitive complexity? How evolution can inform comparative cognition

“…Bumblebees socially learn about nectar robbing and can adaptively reverse a previously learned preference, while honeybees do neither [82]. Bumblebees have larger relative mushroom bodies than honeybees [83]cephalopod Nautilus pompilius, octopus, cuttlefishoctopus and cuttlefish have excellent spatial navigation abilities, short and long-term memory in associative learning tasks, their brains have vertical lobes (where learning and memory are processed), and they are highly mobile and pursue mobile, patchily distributed prey when compared with the nautilus which has poor long-term memory, lacks vertical lobes, and forages by scavenging [84–86]…”

Flexible Spatial Orientation and Navigational Strategies in Chambered Nautilus

“…), although it is larger than any other non‐cephalopod molluscan brain. Contrary to the persistent assumption that their behaviour must also be far simpler than that of coleoids, recent studies show considerable plasticity of behaviour in nautilus (Crook & Basil ; Soucier & Basil ; Crook et al. ; Grasso & Basil ).…”

Invertebrate Models for Biomedical Research, Testing, and Education

“…The chambered nautilus (Nautilus pompilius), one of the most ancient cephalopods, has been used in Pavlovian conditioning studies (Crook and Basil 2008), and Aplysia and H. crassicornis have been used to study classical and operant conditioning (Baxter and Byrne 2006). Studies in Aplysia have led to elucidation of the molecular mechanisms involved in all phases of implicit memory (Hawkins et al 2006), and the mud fl at crab (Chasmagnathus convexus) has served as a model in similar studies (Romano et al 2006).…”