Invertebrate learning. Learning. Associative learning. Why study learning in Invertebrates? 1/30/2013
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1 Why study learning in Invertebrates? Invertebrate learning Invertebrates use learning to adapt to their environment, despite their limited amount of neurons The basic mechanisms supporting neuronal plasticity are similar across genera they can be used as a model to understand human learning mechanisms Learning Learning = durable change in behavior acquired through individual experience Learning is about extracting predictive relationships between events in our environment. It allows extracting the logical structure of our world. Associative learning Learning that 2 or more events are linked together = change in responsiveness resulting from the establishment of a new association between 2 (or more) stimuli Classical conditioning (Pavlov) Operant conditioning (Skinner) 1
2 Basic terminology Unconditioned Stimulus. US A stimulus which elicits and innate reflexive response. Example: Food in the mouth. Unconditioned Response. UR The reflexive response elicited by the US. Example: Salivation. CLASSICAL CONDITIONING Conditioned Stimulus. CS An neutral stimulus which does not initially elicit the UR which will be paired with the US during the experiment. Example: The sound of a bell. Conditioned Response. CR The response occurring to the CS as a result of paired presentations of the US and CS. It may differ in some ways from the UR. Example: Salivation (but, perhaps, of a different composition to the UR). Learning in Aplysia Respiratory system in Aplysia Eric Kandel was granted a Nobel prize in 2000 for his study of learning on Aplysia Gastropod mollusk (sea slug) living along the coast (ex California) Reddish brown soft bodied animal cm long Exhibits defensive withdrawal reflexes readily altered by experience The sea slug Aplysia californica has a siphon, mantle and gill. It breathes by means of oxygen exchange through its gill. Water flows in between the parapodia, under the mantle shelf, over the gill and out through the siphon. 2
3 Retraction reflexes (US) Classical conditioning in Aplysia When a tactile stimulus brushes the mantle shelf or siphon, the gill and siphon are withdrawn into the mantle cavity and covered by the parapodia. CS = weak tactile stimulus to siphon US = Electric shock to tail Pairing the CS US makes CS predict US Cellular analysis Model of how the stimuli used for classical conditioning of the withdrawal reflex of Aplysia induce LTP of sensorimotor synapses together with other associative cellular changes. What is learned? A contingency is established between stimuli = Univocal link between CS and US drives the response The experimenter, not the animal, is in control of the contingency The CS substitutes for the US: CS == US Mediation of Classical Conditioning in Aplysia californica by Long Term Potentiation of Sensorimotor Synapses. Geoffrey G. Murphy, et al. Science 278, 467 (1997); 3
4 Variables in classical conditioning Motivation of the animal CS intensity US intensity Interval between CS and US (interstimulus interval) Number of trials Intertrial intervals Classical conditioning protocols Aplysia classical conditioning Proboscis extension reflex Sting extension reflex media/releases/2004/06/2 5_flies.shtml online.de/de/news Theo Mota, Edith Roussel, Jean-Christophe Sandoz, and Martin Giurfa - Visual conditioning of the sting extension reflex in harnessed honeybees J Exp Biol : Classical conditioning in Drosophila Massed versus spaced conditioning Olfactory Classical Conditioning: Delay, Backwards, Trace conditioning 4
5 Operant conditioning Thorndike s Law of Effect (1905): A response that is reinforced will be repeated A response that is not reinforced will be weakened. OPERANT CONDITIONING Behavior changes because of its consequences = Animals show a tendency to repeat those actions that result in a positive outcome. The operant box: Skinner A controlled environment where animals actively produce actions to obtain reward or avoid punishment What is learned? A contingency between a behavior that is actively produced by the animal and a subsequent reinforcer A discriminative stimulus tells the animal when to respond Informs the animal that a particular action/reinforcement contingency is in effect. 5
6 Just pure operant learning? A flight simulator for Drosophila Behavior > reinforcement = operant Discriminative stimulus > behavior Discriminative stimulus (Sd) > reinforcement Sd > Behav > Ref > Classical and instrumental conditioning combine to influence behavior The fly controls its flight direction to avoid the heated beam punishment Operant conditioning The animal is in control of the reinforcement, contrarily to what happens in classical conditioning It learns to associate a behavior and its consequences Variables in operant conditioning Motivation of the animal Magnitude of the reinforcement Immediacy of the reinforcement Number of trials Intertrial interval 6
7 Operant conditioning protocols Operant conditioning in nature Flight simulator in Drosophila Skinner box for pigeons Woodpecker finchs New Caledonian crows Aplysia feeding? es/h_c_kyllingstad/woodpeckerfinch2.jpg/view.html In Stanley Kubrick's film A Clockwork Orange (based on the novel by Anthony Burgess), the protagonist, Alex, undergoes operant conditioning, or aversion therapy, to modify his (ultra)violent tendencies. cessation as result ofnatural.html Not all learning is elemental HIGHER ORDER FORMS OF LEARNING Not all learning phenomena can be explained on the basis of elemental associations CS US Such univocal links which apply only for the elements linked cannot account for some complex forms of learning 7
8 Learning is based on memory Learning leads to memory, the capacity to store and retrieve information acquired through individual experience. LEARNING AND MEMORY But memories are not made instantaneously by learning; rather, they develop over time and change their properties. Memory has different phases Short term memory (STM): limited in capacity, labile, specific encoding Long term memory (LTM)/ very large capacity, stable, specific encoding Consolidation of STM into LTM is time dependent but STM and LTM are not necessarily sequentially linked Time dependent stages of memory may be based on independent processes acting in parallel Some experimental definitions Between groups definition: The difference in response to the CS in a retention test between a conditioned (CS US paired) and a pseudoconditioned group (CS US unpaired) Or between a conditioned group and a naïve group. Within group definition Absolute conditioning: The difference in response to the CS and a novel stimulus in a retention test Differential conditioning: The difference in response to the CS+ and the CS in a retention test 8
9 Some basic reminders We don t measure memory or learning. Learning and Memory can be only inferred from behavior. We measure the expression of learning and of memory Be careful with the distinction between learning and performance Both analytical (or reductionistic) and synthetic (integrative) approaches are important to understand learning & memory. Simplicity is seductive, and sometimes wrong HABITUATION Habituation Classic definition: A basic form of respondent learning, in which there is a decrease in the strength of a given action after repeated presentation of a stimulus that elicits the response spontaneous recovery and dishabituation and dependence of habituation upon stimulus frequency and stimulus intensity Use in chemical ecology: «habituation» to plant deterrents and induction of preference toward the plant (odors, taste). Habituation in Lepidoptera Adaptation to a host plant on which females have laid their eggs. It involves a host of physiological changes, including the expression of detoxification enzymes and processes to counteract the plant defense. Pending question: when larvae are habituated to a host plant, will the adults choose this host plant? This question is still open 9
10 Other paradigms? CTA: conditioned taste aversion MALAISE ASSOCIATIONS Animals are able to associate a new taste / odor with a digestive malaise occuring even several hours after ingestion. This memory is very stable and involves different circuits in Vertebrates Associative learning & malaise Do flies discriminate LiCl vs NaCl? taste + toxicity = memory? LiCl + sucrose NaCl + sucrose Mean consumption per fly (µl) sucrose 0,20M LiCl 0,19M sucrose 0,20M NaCl 0,19M n= min spk/s * * ** NaCl + sucrose LiCl + sucrose L5 sensillum Salt (M) M sucrose 10
11 Sickness induced by LiCl (1) Sickness induced by LiCl (2) 40 min Exposure to 0.2 M LiCl or NaCl (+ 0.2 M sucrose) 0.4 µl per fly 0.3 N=9 LiCl or NaCl (0.2 M M sucrose) sickness after 60 min Time (min) Recovery after 7h 9h; no significant mortality Post exposure test (+ 1d) Post exposure choice (+48 h) 22h after LiCl exposition 22h after NaCl exposition 42h after LiCl exposition 42h after NaCl exposition Mean consumption per fly (µl) n=9 sucrose LiCl sucrose NaCl Mean consumption per fly (µl) n=9 sucr 0,20M LiCl 0,19M sucr 0,20M NaCl 0,19M Length of the test Lenght of the test (min) 22 h starvation (water) 40 min exposure LiCl or NaCl + sucrose 22 h recovery (water) 40 min test Binary choice 22 h starvation 40 min LiCl or NaCl 7 h 13 h food 22 h 40 min test Binary choice 11
12 How do insects cope with toxic molecules? Honeybee learning Experimental protocol: Postingestive mechanisms Pre-ingestive mechanisms Present an odor, then give them a small quantity of sugar solution mixed with: Quinine: bitter Amygdaline: no taste but liberating HCN in the gut (compound present in the nectar of almond trees) Detoxification Elimination = P450, etc Malaise? Avoidance = Bitter taste Sugar inhib. Bees learn to associate an odor with a taste: the odor becomes a predictor Dec 16, 2010 Aversive Taste in Drosophila DIF 51 12
13 2 different memories Learning quinine involves dopamine Learning amygdaline involves 5 HT (serotonine). Conclusions Learning is found in all animals. It allows to adapt their behavior to their environment and to take into account their experience. Learning is a buzzword for many processes which are qualitatively different. Ultimately, learning involves plasticity in the connectivity between neurons, and neurons which integrate information from different sources (external, internal). Cost of memory Selection of flies based on learning abilities Check that they perform better in a learning paradigm Test their fitness LEARNING CAPABILITIES AND EVOLUTION (expériences Frédéric Méry, LEGS, CNRS Gif sur Yvette) 13
14 Selection procedure Evolution of the oviposition choices Fitness: larvae Mean larval competitive ability of the high learning lines (which had evolved an improved learning ability) and low learning lines (not selected for learning), on three quantities of food: (a) 125 mg of yeast; and (c) 25 mg of yeast. Open bars, original selection lines; grey bars, crosses between different replicate lines ithin selection regimes. Error bars indicate ±1 s.e. Conclusion Learning has an adaptative value But it comes with a cost that affects fitness 14
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