Computation in the Learning System of Cephalopods

Abstract

The memory mechanisms of cephalopods consist of a series of matrices of intersecting axes, which find associations between the signals of input events and their consequences. The tactile memory is distributed among eight such matrices, and there is also some suboesophageal learning capacity. The visual memory lies in the optic lobe and four matrices, with some re-exciting pathways. In both systems, damage to any part reduces proportionally the effectiveness of the whole memory. These matrices are somewhat like those in mammals, for instance those in the hippocampus. The first matrix in both visual and tactile systems receives signals of vision and taste, and its output serves to increase the tendency to attack or to take with the arms. The second matrix provides for the correlation of groups of signals on its neurons, which pass signals to the third matrix. Here large cells find clusters in the sets of signals. Their output re-excites those of the first lobe, unless pain occurs. In that case, this set of cells provides a record that ensures retreat. There is experimental evidence that these distributed memory systems allow for the identification of categories of visual and tactile inputs, for generalization, and for decision on appropriate behavior in the light of experience. The evidence suggests that learning in cephalopods is not localized to certain layers or "grandmother cells" but is distributed with high redundance in serial networks, with recurrent circuits.

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

“…The lack of information on behaviour in nautilus represents a gap in our knowledge of learning among the molluscs, yet nautilus is a particularly interesting subject for studies of the evolution of dedicated learning structures, primarily because of its close relationship to the coleoids, the most neurologically complex invertebrates. It is the oldest and most primitive of the extant cephalopods (Saunders et al, 1996) and is the only extant cephalopod lacking the vertical lobe complex (Young, 1965;Young, 1991). Therefore identifying similar behavioural abilities in nautilus to those known in other cephalopod and non-cephalopod molluscs should shed considerable light on the evolutionary pathways that led to the development of the complex coleoid brain, and on general principles underlying the evolution of neural complexity.…”

“…The thirteen main lobes are not clearly differentiated from the surrounding tissue (Young, 1965) and there appears to be little specialisation. The vertical and subfrontal lobes, regions of the brain that have been implicated in tactile and visual learning and memory in coleoids (Young, 1960;Young, 1961;Hochner et al, 2003) are entirely absent from the nautilus CNS (Young, 1965), and there is some evidence that the structural simplicity of the brain may be representative of an ancestral condition (Young 1991;Shigeno et al, 2007).…”

Distribution of glutamic acid decarboxylase immunoreactivity within the brain of oval squid Sepioteuthis lessoniana

“…Various researchers have suggested that this tract, which shows a matrix-like organization between the vertical lobe, appears to be analogous to vertebrate brain structures involved in learning and memory (e.g. the hippocampus and cerebellum) (Young 1995), and to insect mushroom bodies (Young & Boycott 1955, Young 1991, Hochner et al 2006, Hochner 2010. Among cellular processes, a robust, activitydependent long-term potentiation (LTP) underlying the physiological basis of learning and memory that resembles some aspects of vertebrate LTP is shown in this tract.…”

“…Reports of relationships between sociality and neuronal mechanisms in invertebrates are scarce. However, the GABAergic elements expressed in the tract between the superior frontal lobe and the vertical lobe may play a role in cognitive behaviors such as social interaction, because there are similarities between the hippocampus of the vertebrate brain and the vertical lobe of the cephalopod brain in which abundant GABAergic elements were detected (Young 1991, Hochner et al 2003.…”

Cognitive ability and sentience: Which aquatic animals should be protected?

“…There is also some indication that the nociceptor rate of firing or sensitivity is related to the sensitivity of the tissue that they protect (Mather 2004). Cephalopods can learn to avoid putatively painful stimuli (Young 1991), and have many of the neurotransmitters that are involved in vertebrate pain reception and mediation (Abbott et al 1995).…”