The hare and the snail: Dissociating visual orienting from conscious perception

A method for investigating attentional effects of peripheral visual objects, independently of perceptual identification, is described. We report an experiment using this method which shows that visual processing of peripheral objects differs radically, depending on whether participants move attention in response to an object or consciously perceive that object. When luminance contrast was reduced, conscious perceptual discrimination of peripheral letters was massively slower and less accurate—but both low and high contrast letters elicited rapid attentional orienting effects and these rapid orienting effects were equal in magnitude across low and high contrast. This pattern is consistent with known differences in luminance sensitivity between the dorsal and ventral visual processing streams, and with rapid dorsal–ventral interaction mediated via re-entrant feedback. Our findings show that the control system responsible for rapid movements of attention is exquisitely sensitive to visual form information at low levels of contrast, and involves a different neurocognitive pathway to that which gives rise to conscious perception.     

The interactions of courtship, feeding, and locomotion in the behavioral hierarchy of the snail Helix aspersa

Starvation both increased the number of snails that exhibited feeding (i.e., increased feeding proclivity) and decreased the latencies of response to a food stimulus (i.e., increased food arousal). Feeding inhibited locomotion, although starvation itself had no effect. Sexual arousal (the intensity of courtship) increased locomotion, but only in the absence of a mating partner. Sexual proclivity (the likelihood of a snail to court with conspecifics) had no effect on locomotion. In general, proclivity and arousal had different effects on behavior. Food deprivation did not alter the preference of sexually aroused snails for sexual stimuli over food stimuli Both starved and fed courting pairs responded to a food stimulus only during periods of low sexual arousal, although when not sexually aroused, starved snails usually increased the amount of time they spent in contact with a food stimulus. These results suggest that courtship can suppress feeding and that the expression of feeding behavior is dependent upon the occurrence of low levels of sexual arousal (time sharing).     

Goal-tracking behavior in the pond snail, Lymnaea stagnalis

The occurrence of goal-tracking, an unconditioned stimulus (US)-directed autoshaping behavior, was studied in open-field tests with control and classically conditioned pond snails, Lymnaea stagnalis. In an appetitive classical conditioning paradigm with a tactile stimulus as conditioned stimulus (CS) and a localized food stimulus as US a conditioned feeding response built up in the experimental but not in the control animals. In the post-training open-field tests the experimental group alone showed an enhanced attraction toward the source of water current in the environment which previously signalled the arrival of the US but did not act as CS in the classical conditioning procedure. We suggest that this stimulus-directed goal-tracking behavior in Lymnaea is the result of a classical-operant interaction, described so far only in vertebrate animals, and that neurophysiological analysis of this behavior is possible in this snail.     

Food arousal in the pond snail, Lymnaea stagnalis

Factors affecting food arousal were examined in a behavioral study of the freshwater, browsing pulmonate, Lymnaea stagnalis. Presentation of a food stimulus (sucrose) leads to a progressive decrease in interbite interval over the first four subsequent bites. This is thought to represent an increase in food-induced arousal. The latency to first bite is correlated with total number of bites in the first 5 min following application of food. Latency to bite is significantly reduced for up to 15 min following a brief food stimulus. Previous levels of food consumption do not significantly affect latency to bite (i.e., food responsiveness). However, hunger does lead to an increase in spontaneous biting activity in the absence of food (i.e., food search activity). Latency to bite is negatively correlated with a more general measure of behavioral arousal, the Behavioral State Score. These results are discussed in relation to previous work on other gastropod species. It is concluded that mechanisms of food arousal are adapted to the animal's habitat and life-style.     

Context specificity of latent inhibition in the snail Cornu aspersum

Animal Cognition - The present study was conducted to assess the context specificity of latent inhibition (LI) in the snail Cornu aspersum, using the appetitive Pavlovian Conditioning procedure of...     

"Central arousal" and sexual responsiveness in the snail, Helix aspersa

In molluscs, a "central arousal" system is thought to positively modulate both an animal's level of activity and its behavioral responsiveness. This hypothesis is examined in Helix aspersa by testing the relationships between activity, feeding, and sexual behavior. Activity, feeding, and mating exhibit parallel daily rhythms. Snails are most active, and eat and mate most frequently, during scotophase and the first 3 h of photophase. Handling and injections of serotonin (5 x 10(-7) m/kg body wt) increase general activity. Inducing activity during late photophase increases food consumption, but it does not induce sexual activity. Moreover, serotonin and handling have no effect on sexual arousal; treated snails show no increase in genital eversion stage and require the same length of courtship as controls. If snails are sexually deprived, increasing activity in late photophase does increase copulation frequency, but snails do not copulate more frequently than do unhandled snails tested during early photophase. These results suggest that while manipulations thought to increase central arousal do increase activity and responsiveness to food stimuli, they do not directly affect sexual proclivity or sexual arousal. Moreover, the relationship between feeding and sexual behavior differs between Helix and Aplysia. This difference between the two species may be related to the differences in their reproductive strategies.     

Conditioned taste aversion with sucrose and tactile stimuli in the pond snail Lymnaea stagnalis

A new form of taste aversion conditioning was established in the pond snail Lymnaea stagnalis. An associative memory, lasting 24h, was produced in the pond snail with 20 pairings of 100 mM sucrose as the conditioned stimulus (CS) and mechanical stimulation to the head as the unconditioned stimulus (UCS). Animals exposed to reverse pairings of the CS and UCS failed to learn the association. The learning was characterized by a shift in the response to the UCS from a whole-body withdrawal response to the cessation of feeding behavior.     

Dissociation of sexual arousal and sexual proclivity in the garden snail, Helix aspersa

Sexual arousal (intensity of courtship) and sexual proclivity (tendency to court) in Helix aspersa can be reliably measured using externally observable correlates. Snails with sexual proclivity are significantly more likely to turn toward an anesthetized conspecific after contacting it than are sexually unreceptive snails. Sexual arousal can be inferred from the stage of a snail's genital eversion, which appears only during courtship. The higher the stage of the eversion, the shorter the time required to complete introductory courtship behavior and the higher the rate of successful copulation, the fewer the number of breaks and pauses during courtship, and the longer the time a snail will spend in contact with an anesthetized conspecific. Sexual proclivity has no effect on feeding or locomotory behavior; however, sexual arousal inhibits feeding and increases locomotor activity. Snails that were allowed daily contact with conspecifics required less time to complete introductory courtship behavior relative to snails that were isolated from conspecifics for 1 week. This suggests that daily contact increases sexual arousal. A greater percentage of isolated snails exhibited courtship behavior than did snails which had experienced daily conspecific contact. This suggests that isolation increases sexual proclivity. These differences indicate that sexual arousal is not merely due to an increase in sexual proclivity.     

Appetitive learning using visual conditioned stimuli in the pond snail, lymnaea

Feeding can be conditioned in the pond snail Lymnaea stagnalis to two different visual stimuli (a black panel or a 5-mm black and white check surround) by pairing the potential conditioned stimulus (CS) with sucrose. Exclusion of chemical cues (associated with differences between the water in home tank and that in training apparatus) that could serve as CS is important for successful visual conditioning. A featureless gray surround, used as an alternative to the check (to which it was matched in luminance) in counterbalanced training designs, was discriminated from the check, showing that resolution (for which the eyes would be necessary) was occurring. The gray surround was largely ineffective as a CS. Single-trial learning was possible with the black panel, but not with the check; it is argued that this may be due to lack of prior experience of stimuli like the check. Conditioning of feeding has now been obtained in Lymnaea to chemical, tactile, and visual cues, opening the way to comparative studies of the neural circuitry underlying appetitive conditioning in different senses, so far explored in Lymnaea only for tactile CS. Such comparative studies are as yet largely lacking in invertebrates.     

Reconsolidation of a context long-term memory in the terrestrial snail requires protein synthesis

We investigated the influence of the protein synthesis blocker anisomycin on contextual memory in the terrestrial snail Helix. Prior to the training session, the behavioral responses in two contexts were similar. Two days after a session of electric shocks (5 d) in one context only, the context conditioning was observed as the significant difference of behavioral response amplitudes in two contexts. On the day following testing of context learning, a session of "reminding" was performed, immediately after which the snails were injected with anisomycin or vehicle. Testing of long-term context memory has shown that only anisomycin injections impaired the context conditioning. In control series, the snails were injected after the training session with anisomycin/saline without reminding, and no impairment of the long-term context memory was observed, while injection of anisomycin during the training session completely abolished the long-term memory. No effects of anisomycin on the short-term memory were observed. Surprisingly, injection of anisomycin after the reminding combined with reinforcing stimuli elicited no effect on the context memory. Differences between single-trial and multisession learning are discussed.     

Blocking of conditioning of tentacle lowering in the snail (Helix aspersa)

Experiment 1 established the effectiveness of an appetitive conditioning of odours procedure with snails (Helix aspersa) that was subsequently used for the study of blocking. In this important phenomenon, the conditioning of a CS1 (where CS is the conditioned stimulus) prior to conditioning of a compound, CS1CS2, blocked the conditioning to the CS2. Experiments 2a, 2b, and 2c demonstrated this associative effect using three different experimental controls. Experiments 3a and 3b replicated the blocking effect and allowed us to reject an explanation of blocking based on generalized effects of several treatments of diverse stimuli in blocking and control groups (the pseudoblocking effect). The implications of these results for the study of invertebrate cognition by means of conditioning techniques are discussed.     

A systems approach to the cellular analysis of associative learning in the pond snail Lymnaea

We show that appetitive and aversive conditioning can be analyzed at the cellular level in the well-described neural circuitries underlying rhythmic feeding and respiration in the pond snail, Lymnaea stagnalis. To relate electrical changes directly to behavior, the snails were first trained and the neural changes recorded at multiple sites in reduced preparations made from the same animals. Changes in neural activity following conditioning could be recorded at the level of motoneurons, central pattern generator interneurons and modulatory neurons. Of significant interest was recent work showing that neural correlates of long-term memory could be recorded in the feeding network following single-trial appetitive chemical conditioning. Available information on the synaptic connectivity and transmitter content of identified neurons within the Lymnaea circuits will allow further work on the synaptic and molecular mechanisms of learning and memory.     

A single serotonergic modulatory cell can mediate reinforcement in the withdrawal network of the terrestrial snail

A cluster of 40 serotonergic cells in the rostral part of pedal ganglia of the terrestrial snail Helix lucorum was shown previously to participate in the modulation of withdrawal behavior and to be necessary during the acquisition of aversive withdrawal conditioning in intact snails. Local extracellular stimulation of the serotonergic cells paired with a test stimulus elicited a pairing-specific increase (the difference between paired and explicitly unpaired sessions was significant, p <.01) of synaptic responses to test stimulation in the premotor interneurons involved in withdrawal. This result suggested participation of serotonergic cells in mediating the reinforcement in the withdrawal network. Intracellular stimulation of only one identified Pd4 cell from the pedal group of serotonergic neurons paired with a test stimulus also significantly increased (the difference between paired and explicitly unpaired sessions was significant, p <.05) synaptic responses to paired nerve stimulation in same premotor interneurons involved in withdrawal. Morphological investigation of a cluster of pedal serotonergic neurons showed that only the Pd4 cell had branches in the parietal ganglia neuropile where the synapses of premotor withdrawal interneurons and of presynaptic neurons are located. The data suggest that a single serotonergic cell can mediate the reinforcement in the withdrawal network of the terrestrial snail. Patterns of responses of the Pd4 cells to tactile and chemical stimuli conform to the suggestion.     

Low environmental calcium blocks long-term memory formation in a freshwater pulmonate snail

The freshwater snail Lymnaea stagnalis (L.) is considered a calciphile and exhibits reduced growth and survival in environments containing less than 20 mg/l environmental calcium. Although it has no apparent effect on survival at 20 mg/l, reducing environmental calcium increases metabolic demand, and as such we consider that this level of calcium acts as a stressor on the snail. We exposed snails to acute periods of low environmental calcium and tested their ability to form intermediate-term memory (ITM) and long-term memory (LTM) following one trial operant conditioning (1TT) to reduce aerial respiratory activity in hypoxic conditions. We also assessed whether there were changes in the electrophysiological properties of a single neuron, right pedal dorsal 1 (RPeD1), which has been demonstrated to be necessary for LTM formation. Following training in high (80 mg/l) environmental calcium, L. stagnalis formed ITM and LTM lasting 24 h and demonstrated a significant reduction in all activity measured from RPeD1; however when snails were exposed to low (20 mg/l) environmental calcium they were able to form ITM but not LTM. Although no behavioral LTM was formed, a partial reduction in RPeD1 activtiy measured 24 h after training was observed, indicating a residual effect of training. The strong effect that environmental calcium concentration had on physiology and behavior in response to training to reduce aerial respiration in L. stagnalis suggests that it is an element of gastropod husbandry that needs to be carefully considered when studying other traits. This study also indicates that L. stagnalis found naturally in low calcium environments may be less able to adapt to novel stressors than populations found in harder waters.