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Experimental field study of spatial memory and learning in wild capuchin monkeys (Cebus capucinus).

Despite a large body of data on diet and ranging patterns in prosimians, monkeys and apes, little is known regarding the types of information that non-human primates use when making foraging decisions. In a series of controlled field experiments, we tested the ability of wild capuchins (Cebus capucinus) at La Suerte Biological Research Station in north-eastern Costa Rica to remember the spatial positions of 13 feeding platforms and use olfactory and visual cues to identify baited (real bananas) versus sham (plastic bananas) feeding sites. The results indicate that when 'place' was predictable, the capuchins learned the spatial locations of food and non-food sites rapidly (one-trial learning). In a second experiment, the positions of baited feeding sites were random. In the absence of other information, the capuchins used the presence of a local landmark cue (yellow block) placed at reward platforms to select feeding sites. In a final experiment, there was evidence that expectations regarding the amount of food available at a platform (2 bananas vs. 1/2 banana) had a significant influence on capuchin foraging decisions. Although the capuchins were sensitive to changes in experimental conditions, when they were given conflicting cues, spatial information was predominant over other information in selecting feeding sites.

Animals↗

Spike timing, synchronization and information processing on the sensory side of the central nervous system.

To what extent is the variability of the neuronal responses compatible with the use of spike timing for sensory information processing by the central nervous system? In reviewing the state of the art of this question, I first analyze the characteristics of this variability with its three elements: synaptic noise, impact of ongoing activity and possible fluctuations in evoked responses. I then review the recent literature on the various sensory modalities: somato-sensory, olfactory, gustatory and visual and auditory processing. I emphasize that the conditions in which precise timing, at the millisecond level, is usually obtained, are conditions that usually require dynamic stimulation or sharp changes in the stimuli. By contrast, situations in which stimulation not belonging to the temporal domain is temporally encoded lead to much coarser temporal coding; although in both cases, neural networks transmit the signals with similarly high precision. Synchronization among neurons is an important tool in information processing in both cases but again seems to act either at millisecond or tens of millisecond levels. Information theory applied to both situations confirms that the average rate of information transmission is much higher in dynamic than in static situations. These facts suggest that channels of precise temporal encoding may exist in the brain but imply populations of neurons working in a yet to be discovered way.

Animals↗

Maternal experience influences the establishment of visual/auditory, but not olfactory recognition of the newborn lamb by ewes at parturition.

Maternal behavior in sheep is characterized by the rapid establishment of individual recognition of the lamb through the use of different sensory modalities. Olfactory recognition mediates acceptance at suckling whereas visual/auditory cues are involved in recognition from a distance. This study investigates (a) the timing of both types of recognition and (b) whether they can be influenced by maternal experience. Olfactory recognition was assessed at lambing, 30 min, 1, 2, or 4 hr postpartum by presenting successively an alien and the familiar lamb. Recognition at a distance was assessed at 6, 8, and 12 hr postpartum by using a two-choice test between the familiar and an alien lamb. A majority (33/51) of ewes showed selectivity at suckling as early as 30 min after parturition, and no differences due to maternal experience were observed. By contrast, in the two-choice recognition test, multiparous ewes showed a preference for their familiar lamb at 6 hr whereas primiparous mothers did so only after 24 hr of mother-young contact: The performance of biparous mothers was intermediate. Thus, both types of recognition can be rapidly established after parturition, and maternal experience has a differential effect on the dynamics of these learning processes.

Animals↗

Vestibular contribution to spatial orientation. Evidence of vestibular navigation in an animal model.

To determine if animals are capable of utilizing vestibular sensory input for spatial orientation, a six-arm radial maze with a rotating central turntable was constructed. Sprague-Dawley rats were trained on this apparatus by rotating them without visual, auditory, or olfactory cues. Animals were required to locate a reward (located in a constant position relative to the starting position) following random rotations varying from 0 to +/- 360 degrees, growing progressively larger in 60 degrees increments. Normal rats (N = 10) showed a steady improvement in performance over the training and testing period. Bilateral labyrinthectomy (N = 5) produced a profound decrement in that performance (p less than 0.001). When visual cues were added, labyrinthectomized animals improved their performance, but remained significantly below that of normal animals without visual cues (p less than 0.001). Normal animals allowed to use visual cues showed no improvement over their performance without visual cues. The results indicate that rats can utilize vestibular sensory information for navigational purposes. In fact, under these experimental conditions, rats are more successful in utilizing vestibular sensory input for navigation than visual cues.

Animals↗

Diencephalic neuronal activity during acquisition and ingestion of food in sheep.

Single unit recordings were made in the lateral hypothalamic region and ventrobasal thalamus in conscious sheep during presentation of food and feeding. Unit responses to all aspects of testing were observed between the two areas. However, analysis of the data revealed a functional division of unit types between the two regions. Unit responses specific to the sight of food, to the approach of food to the mouth, and during ingestion of food were observed in the lateral hypothalamic area, but not the ventrobasal thalamus. These responses were not associated with specific or generalized movements, non-specific arousal, with olfactory stimulation, or with other oral stimuli. Units responding in association with specific mouth movements or somatosensory stimulation of the face or mouth-parts were observed in the ventrobasal thalamus but not in the lateral hypothalamic area. In the case of movement-related activity, the response was independent of the stimulus inducing the movement, food and non-food stimuli being equally effective. This was also true of the somatosensory responses observed. Two possibilities in relation to this functional division are discussed. Firstly, that the ventrobasal thalamus receives oral sensory afferents which may be associated with the thalamic area for taste. Secondly, that the activity of hypothalamic cells recorded in the sheep is consistent with a role for this area of the brain in the guidance and control of ingestive behaviour in ruminant as well as non-ruminant species.

Animals↗

Evaluation of acute sensory--motor effects and test sensitivity using termiticide workers exposed to chlorpyrifos.

Sensory and motor testing was performed on a group of termiticide workers primarily using chlorpyrifos-containing products to evaluate both the acute effects from current exposure and sensitivity of the measures to detect effects. The study group comprised 106 applicators and 52 nonexposed participants. Current exposure was measured by urinary concentrations of 3,5,6-trichloro-2-pyridinol (TCP) collected the morning of testing. The mean TCP value for the 106 applicators was 200 microg/g creatinine. Participants received 4--5 h of testing and were evaluated using a sensory--motor test battery recommended by a National Institute for Occupational Safety and Health (NIOSH)-sponsored advisory panel to be appropriate for testing effects from pesticide exposures. Measurements testing olfactory dysfunction, visual acuity, contrast sensitivity, color vision, vibrotactile sensitivity, tremor, manual dexterity, eye--hand coordination, and postural stability were analyzed. Study results indicated limited acute effects from exposure to chlorpyrifos using urinary TCP as a measure of current exposure. The effects occurred primarily on measures of postural sway in the eyes closed and soft-surface conditions, which suggests a possible subclinical effect involving the proprioceptive and vestibular systems. Several other tests of motor and sensory functions did not show any evidence of acute exposure effects, although statistically significant effects of urinary TCP on the Lanthony color vision test scores and one contrast sensitivity test score were found. The visual measures, however, were not significant when a step-down Bonferroni correction was applied. Information also is presented on the sensitivity of the measures to detect effects in an occupationally exposed population using standard error of the parameter estimates.

Animals↗

Male mice lacking the gastrin-releasing peptide receptor (GRP-R) display elevated preference for conspecific odors and increased social investigatory behaviors.

Previously, we generated gastrin-releasing peptide receptor null mutant mice (GRP-R-deficient mice), and found that these animals displayed increased non-aggressive social responses in an ordinary social interaction test using a resident-intruder method. In the present study, we examined in more detail the social behaviors of GRP-R-deficient male mice. In social interaction tests, GRP-R-deficient mice showed more social responses, such as sniffing and nosing, relative to wild-type mice, and similar results were obtained whether GRP-R-deficient mice served as intruders or residents. In the same way, they showed more contact behaviors toward an anesthetized conspecific, and less locomotor activity than wild-type mice in a social investigation test toward an anesthetized male mouse. Since olfactory systems play important roles in the social behavior of rodents, olfactory preference tests were conducted in order to evaluate the olfactory properties of GRP-R-deficient mice. The results suggest that no differences exist between wild-type mice and GRP-R-deficient mice in the preference between a novel sawdust odor and their own odor, or that of other male mice. However, GRP-R-deficient mice preferred the odor of other male mice to their own, in contrast to wild-type mice. Furthermore, the preferences of GRP-R-deficient and wild-type mice were not disrupted by intraperitoneal infusion of diazepam (1.5 mg/kg). These results indicate that neither the motion, nor the behavior of conspecifics, nor reduced anxiety lead to the increased non-aggressive social responses and/or social investigatory behaviors in GRP-R-deficient mice. Rather, these latter behaviors may be a consequence of altered cognition of conspecific odors in the mutant mice.

Aggression↗

Two-photon calcium imaging reveals an odor-evoked map of activity in the fly brain.

An understanding of the logic of odor perception requires a functional analysis of odor-evoked patterns of activity in neural assemblies in the brain. We have developed a sensitive imaging system in the Drosophila brain that couples two-photon microscopy with the specific expression of the calcium-sensitive fluorescent protein, G-CaMP. At natural odor concentration, each odor elicits a distinct and sparse spatial pattern of activity in the antennal lobe that is conserved in different flies. Patterns of glomerular activity are similar upon imaging of sensory and projection neurons, suggesting the faithful transmission of sensory input to higher brain centers. Finally, we demonstrate that the response pattern of a given glomerulus is a function of the specificity of a single odorant receptor. The development of this imaging system affords an opportunity to monitor activity in defined neurons throughout the fly brain with high sensitivity and excellent spatial resolution.

Animals↗

Visual modulation of olfactory learning in honeybees.

We use classical conditioning of the honeybee (Apis mellifera) proboscis extension reflex with a visual (A) and an olfactory (X) conditioned stimulus in a blocking paradigm. Typically, learning about one element (X) of a compound (AX) is decreased (blocked) if the other component (A) has previously been rewarded alone. Our results show that visual pretraining did not produce blocking in honeybees: instead, forward pairings of A with a reward increased subsequent learning about X relative to a backward pairing control. This finding violates the independence assumption, which holds that elements of inter-modal compound stimuli change associative strength independently of each other. Furthermore, it is at odds with common theories of conditioning that predict blocking and assume that the elements of a compound stimulus rely on one common internal reinforcing signal. Taking the functional anatomy of the honeybee brain into account, we suggest that vision and olfaction may not rely on the same internal reinforcing signal; compound interactions might thus reflect the wiring of the honeybee nervous system and the biological significance of different sensory modalities during natural behaviour.

Animals↗

Odour-evoked responses to queen pheromone components and to plant odours using optical imaging in the antennal lobe of the honey bee drone Apis mellifera L.

The primordial functional role of honey bee males (drones) is to mate with virgin queens, a behaviour relying heavily on the olfactory detection of queen pheromone. In the present work I studied olfactory processing in the drone antennal lobe (AL), the primary olfactory centre of the insect brain. In drones, the AL consists of about 103 ordinary glomeruli and four enlarged glomeruli, the macroglomeruli (MG). Two macroglomeruli (MG1 and MG2) and approximately 20 ordinary glomeruli occupy the anterior surface of the antennal lobe and are thus accessible to optical recordings. Calcium imaging was used to measure odour-evoked responses to queen pheromonal components and plant odours. MG2 responded specifically to the main component of the queen mandibular pheromone, 9-ODA. The secondary components HOB and HVA each triggered activity in one, but not the same, ordinary glomerulus. MG1 did not respond to any of the tested stimuli. Plant odours induced signals only in ordinary glomeruli in a combinatorial manner, as in workers. This study thus shows that the major queen pheromonal component is processed in the most voluminous macroglomerulus of the drone antennal lobe, and that plant odours, as well as some queen pheromonal components, are processed in ordinary glomeruli.

Animal Communication↗

Effect of post-training unilateral labyrinthectomy in a spatial orientation task by guinea pigs.

The effects of unilateral labyrinthectomy in guinea pigs have been studied on an angular orientation task consisting, in an open field, of running to a hidden goal oriented at 45 degrees with respect to the cephalocaudal axis of the animal placed in a starting-box. The task was conducted in light but in an homogeneous environment, i.e. without visual, auditory or olfactory cues indicating the location of the goal. A second group of animals was submitted to a similar task running to a hidden goal but the place of the goal was indicated by a colored card. All the animals were trained before the lesion and tested in their respective task for 1 month after the lesion. In the task conducted without conspicuous cues, animals were dramatically disturbed. In contrast, animals pretrained in the visually guided task were not impaired after the lesion. These results point out the important role of vestibular information in performing spatial tasks based on angular estimation, since, even if proprioceptive and visuokinesthetic information remain available, subjects seemed not able to maintain a correct angular trajectory. The trajectories being not disturbed in the visually guided task, one can exclude the hypothesis that such deficit was due to a purely motor disturbance.

Animals↗

Augmented prenatal tactile and vestibular stimulation alters postnatal auditory and visual responsiveness in bobwhite quail chicks.

The fact that the sensory systems do not become functional at the same time during early development raises the question of how sensory systems and their respective stimulative histories might influence one another. Previous studies have shown that unusually early visual experience can alter subsequent responsiveness of both the visual system and the earlier developing olfactory and auditory systems. The question remains as to the extent which modified stimulation to an earlier developing system can also result in changes in responsiveness in later developing sensory systems. This study examined the effects of augmented prenatal tactile and vestibular stimulation on bobwhite quail chicks' postnatal visual and auditory responsiveness to maternal cues. Results indicate that augmented prenatal tactile and vestibular stimulation can alter postnatal perceptual responsivensss in the later developing auditory and visual sensory systems. Chicks exposed to augmented prenatal proximal stimulation continued to respond to maternal auditory cues into later stages of postnatal development and failed to demonstrate responsiveness to maternal visual cues in the days following hatching. However, augmented tactile and vestibular stimulation did not appear to affect prenatal auditory learning of an individual maternal call. These findings indicate a strong but selective pattern of influence between the sensory modalities during the prenatal period and support the view that substantially increased amounts of prenatal sensory stimulation can interfere with the emergence of species-typical perceptual functioning.

Animals↗

Measurement of the orbitofrontal cortex: a validation study of a new method.

The orbital frontal cortex (OFC) plays a critical role in the pathophysiology of several neuropsychiatric disorders. Few morphometric neuroimaging studies have examined the OFC using different methodologies and have reported discrepant values. Substantial variability in gyri and sulci across individuals as well as unclear landmarks underline the difficulties in obtaining accurate and reliable measurements. We propose a new geometrical method for measuring the OFC taking into account individual brain variability. The OFC was defined by using the intercommissural line and the inferior edge of the frontal lobe as the main landmarks. The medial and lateral subdivisions of OFC were also separately measured using the olfactory sulcus as the boundary to distinguish between them. After resampling and refitting, 10 scans were independently traced by two trained researchers using BRAINS software. Talairach coordinates were identified on each scan from the OFC and surrounding adjacent brain regions to assess the validity of this method. Brain regions were assigned using Talairach Daemon system. OFC volumes were comparable with those previously reported. Sensitivity and specificity for OFC gray matter were 87.6 and 84.8%, respectively. Intraclass coefficients (ICCs) for gray, white, and total OFC were 0.995, 0.994, and 0.997, respectively. ICCs for OFC medial and lateral subdivisions ranged between 0.996 and 0.998. This method appears to be a valid method for measuring the OFC with excellent reliability. This uncomplicated approach is easy to apply and has the potential to be a valuable alternative to the previously published methods.

Adult↗

Molecular cloning and sequencing of general odorant-binding proteins GOBP1 and GOBP2 from the tobacco hawk moth Manduca sexta: comparisons with other insect OBPs and their signal peptides.

Odorant-binding proteins (OBPs) are small, water-soluble proteins uniquely expressed in olfactory tissue of insects and vertebrates. OBPs are present in the aqueous fluid surrounding olfactory sensory dendrites and are thought to aid in the capture and transport of hydrophobic odorants into and through this fluid. OBPs may represent the initial biochemical recognition step in olfaction, because they transport odorants to the receptor neurons. Insect OBPs are represented by multiple classes: pheromone-binding proteins (PBPs) and general odorant-binding proteins (GOBP1 and GOBP2). PBPs associate with pheromone-sensitive neurons, while GOBPs associate with general odorant-sensitive neurons. Analysis of N-terminal amino acid sequences of 14 insect OBPs isolated from six species indicated that the PBPs were variable and the GOBPs were highly conserved. However, inferred properties of these proteins were based only on partial sequence data. We now report the full-length sequences of a GOBP1 and GOBP2 from the moth Manduca sexta and compare these sequences with those of PBPs from three species, including M. sexta, Antheraea polyphemus, and A. pernyi. We also compare these with a GOBP2 of A. pernyi, previously identified only as a novel OBP. These comparisons fully support our N-terminal analysis. The signal peptide sequences of seven insect OBPs reveal conserved sequences within OBP classes, but not between OBP classes even within the same animal species. This suggests that multiple OBPs may be coexpressed in the same cell type, but differentially processed in a class-specific manner. Properties of the GOBPs suggest that general olfaction is broadly receptive at the periphery. Properties of the PBPs suggest that pheromone olfaction is discriminatory at the periphery, and that the initial biochemical steps in pheromone detection may play an active role in odor perception.

Amino Acid Sequence↗

Different effects of unilateral and bilateral hippocampal lesions in rats on the performance of radial maze and odor-paired associate tasks.

The hippocampus plays an important role in the declarative or explicit memory in humans and is necessary for allocentric spatial learning and olfactory memory in animals. In primates and rodents, the bilateral hemispheres of the brain (especially the forebrain) symmetrically and asymmetrically contribute to diverse cognitive manipulations. In this study, we investigated the role of the hippocampus in spatial memory and in odor-paired associate memory by unilaterally or bilaterally lesioning this region in rats. The bilateral removal, but not the unilateral removal, of the hippocampus impaired both the acquisition of spatial working memory in the radial maze task and the retrieval of maze performance tested 1 month after the acquisition trials. In contrast, neither bilateral nor unilateral removal impaired the odor-paired associate learning. These findings suggest that the hippocampus is critical to the spatial memory, and that a unilateral hippocampus is sufficient for executing a spatial task. The present results also indicate that the hippocampus plays a minor role in odor-dominated associate learning and that some kinds of memories in rats may be processed independently by the left or right hippocampus.

Animals↗

Influenza A virus infection causes alterations in expression of synaptic regulatory genes combined with changes in cognitive and emotional behaviors in mice.

Epidemiological studies have indicated a link between certain neuropsychiatric diseases and exposure to viral infections. In order to examine long-term effects on behavior and gene expression in the brain of one candidate virus, we have used a model involving olfactory bulb injection of the neuro-adapted influenza A virus strain, WSN/33, in C57Bl/6 mice. Following this olfactory route of invasion, the virus targets neurons in the medial habenular, midline thalamic and hypothalamic nuclei as well as monoaminergic neurons in the brainstem. The mice survive and the viral infection is cleared from the brain within 12 days. When tested 14-20 weeks after infection, the mice displayed decreased anxiety in the elevated plus-maze and impaired spatial learning in the Morris water maze test. Elevated transcriptional activity of two genes encoding synaptic regulatory proteins, regulator of G-protein signaling 4 and calcium/calmodulin-dependent protein kinase IIalpha, was found in the amygdala, hypothalamus and cerebellum. It is of particular interest that the gene encoding RGS4, which has been related to schizophrenia, showed the most pronounced alteration. This study indicates that a transient influenza virus infection can cause persistent changes in emotional and cognitive functions as well as alterations in the expression of genes involved in the regulation of synaptic activities.

Animals↗

Elemental and configural learning and the perception of odorant mixtures by the spiny lobster Panulirus argus.

The present study used a conditioning assay to investigate if the type of learning task that spiny lobsters (Panulirus argus) were required to perform influenced the way that they perceived odorant mixtures. Mixtures were composed of 2 food-related compounds (adenosine-5'-monophosphate, betaine, or L-glutamate) at concentrations that produced the same duration of searching behavior in unconditioned animals. Aversive conditioning of search behavior coupled with generalization testing was used to evaluate perceptual similarity between related mixtures. When animals were conditioned to stop searching to a binary mixture AX, they did not generalize significantly from this mixture to either of its components (A or X), or to a binary mixture containing one novel component (AY). However, when lobsters were conditioned to avoid AX but to continue responding to AY, they generalized between AX and X and between AY and Y. The results support the hypothesis that altering the salience of a mixture's components by giving them different reinforcement contingencies changed the way that the mixtures were perceived. As a result of such conditioning, animals perceived the mixture's components as separate elements, rather than as a configuration, and, as a consequence, animals generalized between binary mixtures and their most salient or predictive components.

Animals↗

A naturalistic analysis of autobiographical memories triggered by olfactory visual and auditory stimuli.

The emotional and content qualities of autobiographical memories evoked by three memory cue items (campfire, fresh-cut grass, popcorn) presented in olfactory, visual and auditory form were examined using a new repeated measures paradigm. Results revealed that memories recalled by odors were significantly more emotional and evocative than those recalled by the same cue presented visually or auditorily. However, there were no differences in the content features (vividness, specificity) of memories as a function of cue-form. These findings support previous research in both laboratory and naturalistic settings and is the first comparative sensory memory study to include auditory variants of memory cues. The present data contribute to a growing body of evidence indicating that there is a privileged relationship between olfaction and emotion during recollection. Various subject factors such as age, sex and region of residence were also examined and some were found to affect the quality of memories in interaction with the specific memory cue items, indicating that prior experience is a primary influence in autobiographical memory. Questions for future investigation regarding how odor-evoked memories may be different from other memory experiences are suggested.

Acoustic Stimulation↗