Behavioral and neuronal attributes of short- and long-term habituation in the crab Chasmagnathus

Investigations using invertebrate species have led to a considerable progress in our understanding of the mechanisms underlying learning and memory. In this review we describe the main behavioral and neuronal findings obtained by studying the habituation of the escape response to a visual danger stimulus in the crab Chasmagnathus granulatus. Massed training with brief intertrial intervals lead to a rapid reduction of the escape response that recovers after a short term. Conversely, few trials of spaced training renders a slower escape reduction that endures for many days. As predicted by Wagner’s associative theory of habituation, long-term habituation in the crab proved to be determined by an association between the contextual environment of the training and the unconditioned stimulus. By performing intracellular recordings in the brain of the intact animal at the same time it was learning, we identified a group of neurons that remarkably reflects the short- and long-term behavioral changes. Thus, the visual memory abilities of crabs, their relatively simple and accessible nervous system, and the recording stability that can be achieved with their neurons provide an opportunity for uncovering neurophysiological and molecular events that occur in identifiable neurons during learning.     

Co-induction of long-term potentiation and long-term depression at a central synapse in the leech

Most studies of long-term potentiation (LTP) have focused on potentiation induced by the activation of postsynaptic NMDA receptors (NMDARs). However, it is now apparent that NMDAR-dependent signaling processes are not the only form of LTP operating in the brain [Malenka, R. C., & Bear, M. F. (2004). LTP and LTD: An embarrassment of riches. Neuron, 44, 5–21]. Previously, we have observed that LTP in leech central synapses made by the touch mechanosensory neurons onto the S interneuron was NMDAR-independent [Burrell, B. D., & Sahley, C. L. (2004). Multiple forms of long-term potentiation and long-term depression converge on a single interneuron in the leech CNS. Journal of Neuroscience, 24, 4011–4019]. Here we examine the cellular mechanisms mediating T-to-S (T → S) LTP and find that its induction requires activation of metabotropic glutamate receptors (mGluRs), voltage-dependent Ca²⁺ channels (VDCCs) and protein kinase C (PKC). Surprisingly, whenever LTP was pharmacologically inhibited, long-term depression (LTD) was observed at the tetanized synapse, indicating that LTP and LTD were activated at the same time in the same synaptic pathway. This co-induction of LTP and LTD likely plays an important role in activity-dependent regulation of synaptic transmission.     

Quantity discrimination in Tenebrio molitor: evidence of numerosity discrimination in an invertebrate?

Numerosity discrimination, the ability to distinguish between sets with more and less items, is recognised as the foundation for higher numerical abilities. Understanding numerosity discrimination from a comparative perspective is hence pivotal in tracing the evolution of numerical representation systems. However, numerosity discrimination has been well studied only in vertebrates, where two innate systems of number representation have been described: an ‘analog magnitude system’ used to discriminate among numerosities by representing them as cardinal magnitudes and a ‘parallel individualisation system’ that allows precise discrimination among small arrays of items (≤4) by representing objects individually. We investigated the existence of quantity discrimination in an insect species (Tenebrio molitor) by using a spontaneous two-choice procedure in which males were exposed to substrates bearing odours from different numbers of females (≤4) in increasing numerosity ratios (1:4, 1:3 and 1:2). We show that males can discriminate sources of odours reflecting 1 versus 4 and 1 versus 3 females, but not 2 versus 4 or 1 versus 2, indicating that T. molitor males exhibit a marked preference for sources reflecting more female donors only when numerosity ratios are below 1:2. We discuss the functional significance of this finding and whether our pattern of results could be best explained by summation of a non-numerical continuous variable or by the existence of a numerosity discrimination mechanism with an operational signature ratio of 1:2.     

Cuttlefish (Sepia officinalis: Cephalopoda) hunting behavior and associative learning

Because most learning studies in cephalopods have been performed on octopods, it remains unclear whether such abilities are specific to octopus, or whether they correlate with having a larger and more centrally organized brain. To investigate associative learning in a different cephalopod, six sexually mature cuttlefish (Sepia officinalis) participated in a counterbalanced, within-subjects, appetitive, classical conditioning procedure. Two plastic spheres (conditioned stimuli, CSs), differing in brightness, were presented sequentially. Presentation of the CS+ was followed 5 s later by a live feeder fish (unconditioned stimulus, US). Cuttlefish began to attack the CS+ with the same type of food-acquisition seizures used to capture the feeder fish. After seven blocks of training (42 presentations of each CS) the difference in seizure probability between CS+ and CS– trials more than doubled; and was found to be significantly higher in late versus early blocks. These results indicate that cuttlefish exhibit autoshaping under some conditions. The possible ecological significance of this type of learning is briefly discussed.Electronic Supplementary Material Supplementary material is available for this article at