Learning in honey bees with brain lesions: how partial mushroom-body ablations affect sucrose responsiveness and tactile antennal learning

Honey bees are ideal organisms for studying associative learning, because they can rapidly learn different sensory cues, even under laboratory conditions. Classical olfactory learning experiments have shown that the mushroom bodies (MBs), a prominent neuropil of the central nervous system of the bee, are involved in olfactory learning and memory formation. We tested whether the MBs are also involved in tactile antennal learning. As in olfactory learning, bees use the antennae during tactile learning to sense tactile cues. We produced specific MB ablations by applying the mitotic blocker hydroxyurea (HU). In Drosophila, HU-induced brain lesions of the MBs strongly impaired olfactory memory formation. As treatment with HU might also interfere with the processing of the reward stimulus, sucrose, we measured the responsiveness to sucrose stimuli in these bees. Treatment with HU led to partial ablations of the median MB sub-units on one or both sides of the brain. We analysed side-specific effects in double-blind tests, testing sucrose responsiveness separately for each antenna, and conditioning first one antenna and then the other in a reversal learning assay. HU-treated bees without detectable ablations were less responsive to sucrose and had a poorer learning performance than untreated controls. Partial MB ablation did not additionally affect responsiveness to sucrose or tactile antennal learning. Interestingly, bees with bilateral MB ablations did not differ from untreated controls in their learning performance during the first learning phase. During reversal learning, acquisition in these bees was significantly lower than that in untreated controls. It is concluded that HU treatment affects sucrose responsiveness and tactile learning even without detectable ablation of neuropils. The effects of MB ablations on tactile learning are not side-specific and not correlated with the volume of the ablated neuropil. Accepted after revision: 15 January 2001 ❚ Electronic Publication     

Asymmetrical learning between a tactile and visual serial RT task

According to many researchers, implicit learning in the serial reaction-time task is predominantly motor based and therefore should be independent of stimulus modality. Previous research on the task, however, has focused almost completely on the visual domain. Here we investigated sequence learning when the imperative stimuli were presented tactilely to the fingers. Learning in this task was compared to sequence learning in a typical visual task, using very similar experimental conditions. The results indicate that sequential learning occurs in the tactile task, though to a lesser degree than in its visual counterpart. Furthermore, there was similar cross-modal transfer in both directions, meaning that transfer from the visual to the tactile task was partial. It is proposed that sequence learning involves a stimulus-specific component in the visual but not in the tactile task.     

Asymmetrical learning between a tactile and visual serial RT task

According to many researchers, implicit learning in the serial reaction-time task is predominantly motor based and therefore should be independent of stimulus modality. Previous research on the task, however, has focused almost completely on the visual domain. Here we investigated sequence learning when the imperative stimuli were presented tactilely to the fingers. Learning in this task was compared to sequence learning in a typical visual task, using very similar experimental conditions. The results indicate that sequential learning occurs in the tactile task, though to a lesser degree than in its visual counterpart. Furthermore, there was similar cross-modal transfer in both directions, meaning that transfer from the visual to the tactile task was partial. It is proposed that sequence learning involves a stimulus-specific component in the visual but not in the tactile task.     

Sensory responsiveness and the effects of equal subjective rewards on tactile learning and memory of honeybees

In tactile learning, sucrose is the unconditioned stimulus and reward, which is usually applied to the antenna to elicit proboscis extension and which the bee can drink when it is subsequently applied to the extended proboscis. The conditioned stimulus is a tactile object that the bee can scan with its antennae. In this paper we describe the quantitative relationships between gustatory antennal stimulation, gustatory proboscis stimulation, and tactile learning and memory. Bees are 10-fold more responsive to sucrose solutions when they are applied to the antenna compared to proboscis stimulation. During tactile conditioning, the sucrose solution applied to the proboscis determines the level of acquisition, whereas antennal input is of minor importance. Bees differing in their gustatory responsiveness measured at the antenna differ strongly in their tactile acquisition and memory. We demonstrate how these differences in tactile acquisition and memory can be greatly reduced by calculating equal subjective rewards, based on individual gustatory responsiveness.     

Selective associations in one-day-old rats: taste-toxicosis and texture-shock aversion learning

One-day-old rats learned aversions to a novel taste paired with lithium-induced distress and to a tactile stimulus paired with brief electric shocks. However, aversions did not develop when taste was paired with shock or when the tactile stimulus was paired with lithium treatment. The aversions occurred only when lithium treatment immediately followed taste exposure and when shock was concurrent with exposure to the tactile stimulus. These findings indicate that selective associations in aversion learning are mediated by innate mechanisms that govern conditioning in the absence of extensive ontogenetic experience. The present research also shows that selective associations are sufficient for the occurrence of long-delay learning.     

The effects of genotype, foraging role, and sucrose responsiveness on the tactile learning performance of honey bees (Apis mellifera L.)

We analyzed sucrose responsiveness and associative tactile learning in two genetic strains of honey bees under laboratory conditions. These strains differ in their foraging behavior. Bees of the "high" strain preferentially collect pollen. "Low"-strain bees mainly forage for nectar. Responsiveness to different sucrose concentrations and tactile learning were examined using the proboscis extension reflex. Acquisition, extinction of conditioned responses, and responses to an alternative tactile stimulus were tested. High-strain bees are more responsive to sucrose than low-strain bees. Regardless of genotype, pollen foragers are more responsive to sucrose than nectar foragers. In bees of both strains we find the same relationship between responsiveness to sucrose and acquisition. Bees responding to low sucrose concentrations show more often the conditioned response during acquisition than those responding only to higher sucrose concentrations. Extinction of conditioned responses depends on the response probability during acquisition. Discrimination between the two tactile stimuli is affected by genotype but not by responsiveness to sucrose. High-strain bees discriminate better than low-strain bees. Our experiments thus establish links between division of labor, responsiveness to sucrose, and associative learning in honey bees.     

Sensory feedback in the learning of a novel motor task

The role of different forms of feedback is examined in learning a novel motor task. Five groups of ten subjects had to learn the voluntary control of the abduction of the big toe, each under a different feedback condition (proprioceptive feedback, visual feedback, EMG feedback, tactile feedback, force feedback). The task was selected for two reasons. First, in most motor learning studies subjects have to perform simple movements which present hardly any learning problem. Second, studying the learning of a new movement an provide useful information for neuromuscular reeducation, where patients often also have to learn movements for which no control strategy exists. The results show that artificial sensory feedback (EMG feedback, force feedback) is more powerful than "natural" (proprioceptive, visual, and tactile) feedback. The implications of these results for neuromuscular reeducation are discussed.     

Sensory Feedback in the Learning of a Novel Motor Task

The role of different forms of feedback is examined in learning a novel motor task. Five groups of ten subjects had to learn the voluntary control of the abduction of the big toe, each under a different feedback condition (proprioceptive feedback, visual feedback, EMG feedback, tactile feedback, force feedback). The task was selected for two reasons. First, in most motor learning studies subjects have to perform simple movements which present hardly any learning problem. Second, studying the learning of a new movement can provide useful information for neuromuscular reeducation, where patients often also have to learn movements for which no control strategy exists. The results show that artificial sensory feedback (EMG feedback, force feedback) is more powerful than “natural” (proprioceptive, visual, and tactile) feedback. The implications of these results for neuromuscular reeducation are discussed.     

Lost in the move? Secondary task performance impairs tactile change detection on the body

Change blindness, the surprising inability of people to detect significant changes between consecutively-presented visual displays, has recently been shown to affect tactile perception as well. Visual change blindness has been observed during saccades and eye blinks, conditions under which people’s awareness of visual information is temporarily suppressed. In the present study, we demonstrate change blindness for suprathreshold tactile stimuli resulting from the execution of a secondary task requiring bodily movement. In Experiment 1, the ability of participants to detect changes between two sequentially-presented vibrotactile patterns delivered on their arms and legs was compared while they performed a secondary task consisting of either the execution of a movement with the right arm toward a visual target or the verbal identification of the target side. The results demonstrated that a motor response gave rise to the largest drop in perceptual sensitivity (as measured by changes in d′) in detecting changes to the tactile display. In Experiment 2, we replicated these results under conditions in which the participants had to detect tactile changes while turning a steering wheel instead. These findings are discussed in terms of the role played by bodily movements, sensory suppression, and higher order information processing in modulating people’s awareness of tactile information across the body surface.     

Tactile order memory: evidence for sequence learning phenomena found with other stimulus types

We examine serial order memory for sequences of tactile stimuli and investigate whether established characteristics of order memory, namely serial position effects, error distributions, and Hebb repetition learning, are observed with tactile memory. Visually obscured participants received six tactile stimulations: one to each of six fingers. At test, participants lifted the six fingers in the order of stimulation. For every third trial participants received the same order of stimulation (i.e. the Hebb sequence). Serial recall accuracy produced the canonical bowed serial position function found for immediate serial recall. In addition, recall for the Hebb sequence improved relative to the filler sequences, providing the first demonstration of the Hebb repetition effect with tactile stimuli. Analysis of errors revealed close similarities to that reported with verbal and visual stimuli. This experiment further generalises established features of order memory to tactile memory, supporting the utilisation of an analogous order memory mechanism across stimuli.     

Teaching children with autism spectrum disorder to tact olfactory stimuli

Research on tact acquisition by children with autism spectrum disorder (ASD) has often focused on teaching participants to tact visual stimuli. It is important to evaluate procedures for teaching tacts of nonvisual stimuli (e.g., olfactory, tactile). The purpose of the current study was to extend the literature on secondary target instruction and tact training by evaluating the effects of a discrete‐trial instruction procedure involving (a) echoic prompts, a constant prompt delay, and error correction for primary targets; (b) inclusion of secondary target stimuli in the consequent portion of learning trials; and (c) multiple exemplar training on the acquisition of item tacts of olfactory stimuli, emergence of category tacts of olfactory stimuli, generalization of category tacts, and emergence of category matching, with three children diagnosed with ASD. Results showed that all participants learned the item and category tacts following teaching, participants demonstrated generalization across category tacts, and category matching emerged for all participants.     

Cocaine-induced brainstem seizures and behavior.

A variety of abnormal sensory/motor behaviors associated with electrical discharges recorded from the bilateral brainstem were induced in adult WKY rats by mechanical (electrode implants) and DC electrical current stimulations and by acute and chronic administration of cocaine. The electrode implant implicated one side or the other of the reticular system of the brainstem but subjects were not incapacitated by the stimulations. Cocaine (40 mg/kg) was injected subcutaneously for an acute experiment and subsequent 20 mg/kg doses twice daily for 3 days in a chronic study. Cocaine generated more abnormal behaviors in the brainstem perturbation group, especially the electrically perturbated subjects. The abnormal behaviors were yawning, retrocollis, hyperactivity, hypersensitivity, "beating drum" behavior, squealing, head bobbing, circling, sniffing, abnormal posturing, and facial twitching. Shifts in the power frequency spectra of the discharge patterns were noted between quiet and pacing behavioral states. Hypersensitivity to various auditory, tactile, and visual stimulation was present and shifts in the brainstem ambient power spectral frequency occurred in response to tactile stimulation. These findings suggest that the brainstem generates and propagates pathological discharges that can be elicited by mechanical and DC electrical perturbation. Cocaine was found to activate the discharge system and thus induce abnormal behaviors that are generated at the discharge site and at distant sites to which the discharge propagates. Cognitive functions may also be involved since dopaminergic and serotonergic cellular elements at the brainstem level are also implicated.     

Tactile learning is task specific but transfers between fingers

Practice-related improvement in visual perception is highly specific for properties of the stimulus used in training. We explored the specificity of such perceptual learning in the human tactile system, using gratings consisting of alternating ridges and grooves. Practice effects on grating discrimination showed limited transfer between grating sets defined by spatial variation in either groove width or ridge width, consistent with partially overlapping neural representations of these two spatial parameters. In contrast, substantial interdigital transfer of practice effects occurred for discrimination of gratings varying in either spatial parameter and also for spatial acuity-dependent discrimination of grating orientation. We conclude that tactile learning, although quite as task specific as in other sensory systems, generalizes with considerable facility across fingers, unlike visual learning, which is highly location specific.     

Cortical plasticity associated with Braille learning

Blind subjects who learn to read Braille must acquire the ability to extract spatial information from subtle tactile stimuli. In order to accomplish this, neuroplastic changes appear to take place. During Braille learning, the sensorimotor cortical area devoted to the representation of the reading finger enlarges. This enlargement follows a two-step process that can be demonstrated with transcranial magnetic stimulation mapping and suggests initial unmasking of existing connections and eventual establishment of more stable structural changes. In addition, Braille learning appears to be associated with the recruitment of parts of the occipital, formerly `visual', cortex (V1 and V2) for tactile information processing. In blind, proficient Braille readers, the occipital cortex can be shown not only to be associated with tactile Braille reading but also to be critical for reading accuracy. Recent studies suggest the possibility of applying non-invasive neurophysiological techniques to guide and improve functional outcomes of these plastic changes. Such interventions might provide a means of accelerating functional adjustment to blindness.     

Cocaine-induced brainstem seizures and behavior

A variety of abnormal sensory/motor behaviors associated with electrical discharges recorded from the bilateral brainstem were induced in adult WKY rats by mechanical (electrode implants) and DC electrical current stimulations and by acute and chronic administration of cocaine. The electrode implant implicated one side or the other of the reticular system of the brainstem but subjects were not incapacitated by the stimulations. Cocaine (40 mg/kg) was injected subcutaneously for an acute experiment and subsequent 20 mg/kg doses twice daily for 3 days in a chronic study. Cocaine generated more abnormal behaviors in the brainstem perturbation group, especially the electrically perturbated subjects. The abnormal behaviors were yawning, retrocollis, hyperactivity, hypersensitivity, “beating drum” behavior, squealing, head bobbing, circling, sniffing, abnormal posturing, and facial twitching. Shifts in the power frequency spectra of the discharge patterns were noted between quiet and pacing behavioral states. Hypersensitivity to various auditory, tactile, and visual stimulation was present and shifts in the brainstem ambient power spectral frequency occurred in response to tactile stimulation. These findings suggest that the brainstem generates and propagates pathological discharges that can be elicited by mechanical and DC electrical perturbation. Cocaine was found to activate the discharge system and thus induce abnormal behaviors that are generated at the discharge site and at distant sites to which the discharge propagates. Cognitive functions may also be involved since dopaminergic and serotonergic cellular elements at the brainstem level are also implicated.     

A comparison of neuronal reactions during classical and instrumental conditioning under similar conditions

During the elaboration of an instrumental reflex, it is not obligatory to use a conditioned stimulus, which signals the necessity to generate an instrumental reaction in order to receive reinforcement. However, the presence of a conditioned stimulus simplifies analysis of instrumental reaction, which in this case is the response to the conditioned stimulus. On the other hand, it is necessary to distinguish between instrumental and classical conditioning, since in both cases the response to a conditioned stimulus increases. We studied neuronal analogs of classical and instrumental conditioning in the identified neurons responsible for the defensive closure of the pneumostome in the Helix mollusk under the same conditions. During classical conditioning, a mollusk received punishment after a tactile stimulus. During instrumental conditioning, a mollusk received punishment when an identified neuron did not generate an action potential in response to a tactile stimulus. The appearance of a painful stimulus did not depend on the generation or failure of a spike in the related control neuron. Another tactile stimulus, which was never paired with an unconditioned stimulus, was used as a discriminated stimulus. We also compared the behavior of such identified neurons during pseudoconditioning. The experiments were carried out in a semi-intact preparation. We examined how responses to the tactile and painful stimuli changed during different forms of training. It was shown that the dynamics of neuronal responses to a conditioned tactile stimulus were much more complex during instrumental conditioning and consisted of several phases. Throughout a learning session, neural system consecutively acquired information as to which kind of learning was presented, whether a reaction of the neural system must be generated or inhibited and which instrumental reaction is correct. We have demonstrated that response to a painful stimulus during classical conditioning decreases after short-term initial increase. However, during instrumental learning, the neurons controlling instrumental action remained highly sensitive to the unconditioned stimulus. Meanwhile, foreign neurons decreased their responses to the unconditioned stimulus. We may tentatively conclude that classical and instrumental paradigms are fundamentally different at the cellular level.     

Tactile perception in blind Braille readers: a psychophysical study of acuity and hyperacuity using gratings and dot patterns

It is not clear whether the blind are generally superior to the sighted on measures of tactile sensitivity or whether they excel only on certain tests owing to the specifics of their tactile experience. We compared the discrimination performance of blind Braille readers and age-matched sighted subjects on three tactile tasks using precisely specified stimuli. Initially, the blind significantly outperformed the sighted at a hyperacuity task using Braille-like dot patterns, although, with practice, both groups performed equally well. On two other tasks, hyperacute discrimination of gratings that differed in ridge width and spatial-acuity-dependent discrimination of grating orientation, the performance of the blind did not differ significantly from that of sighted subjects. These results probably reflect the specificity of perceptual learning due to Braille-reading experience.     

Somatosensory processes subserving perception and action

The functions of the somatosensory system are multiple. We use tactile input to localize and experience the various qualities of touch, and proprioceptive information to determine the position of different parts of the body with respect to each other, which provides fundamental information for action. Further, tactile exploration of the characteristics of external objects can result in conscious perceptual experience and stimulus or object recognition. Neuroanatomical studies suggest parallel processing as well as serial processing within the cerebral somatosensory system that reflect these separate functions, with one processing stream terminating in the posterior parietal cortex (PPC), and the other terminating in the insula. We suggest that, analogously to the organisation of the visual system, somatosensory processing for the guidance of action can be dissociated from the processing that leads to perception and memory. In addition, we find a second division between tactile information processing about external targets in service of object recognition and tactile information processing related to the body itself. We suggest the posterior parietal cortex subserves both perception and action, whereas the insula principally subserves perceptual recognition and learning.     

Bidirectional lexical-gustatory synesthesia

In developmental lexical–gustatory synesthesia, specific words (inducers) can trigger taste perceptions (concurrents) and these synesthetic associations are generally stable. We describe a case of multilingual lexical–gustatory synesthesia for whom some synesthesias were bidirectional as some tastes also triggered auditory word associations. Evoked concurrents could be gustatory but also tactile sensations. In addition to words and pseudowords, many voices were effective inducers, suggesting increased connections between cortical taste areas and both voice-selective and language-selective areas. Lasting changes in some evoked tastes occurred during childhood suggesting that some plasticity can be present after the initial learning of associations. Inducers were often linked to taste concurrents phonologically or semantically, but also through identifiable childhood episodes (persons or events). Several inducers were phonologically linked to episodic inducers suggesting a process of secondary acquisition for many inducers. Implications of these observations are discussed.     

Attention and suppression affect tactile perception in reach-to-grasp movements

Reaching with the hand is characterized by a decrease in sensitivity to tactile stimuli presented to the moving hand. Here, we investigated whether tactile suppression can be canceled by attentional orienting. In a first experiment, participants performed a dual-task involving a goal-directed movement paired with the speeded detection of a tactile pulse. The pulse was either delivered to the moving or stationary hand, during movement preparation, execution, or the post-movement phase. Furthermore, stimulation was delivered with equal probability to either hand, or with a higher probability to either the moving or resting hand. The results highlighted faster RTs under conditions of higher probability of stimulation delivery to both moving and resting hands, thus indicating an attentional effect. For the motor preparation period, RTs were faster only at the resting hand under conditions where tactile stimulation was more likely to be delivered there. In a second experiment, a non-speeded perceptual task was used as a secondary task and tactile discrimination thresholds were recorded. Tactile stimulation was delivered concomitantly at both index fingers either in the movement preparation period (both before and after the selection of the movement effector had taken place), in the motor execution period, or, in a control condition, in the time-window of motor execution, but the movement of the hand was restrained. In the preparation period, tactile thresholds were comparable for the two timings of stimulation delivery; i.e., before and after the selection of the movement effector had taken place. These results therefore suggest that shortly prior to, and during, the execution of goal-directed movements, a combined facilitatory and inhibitory influence acts on tactile perception.