Insect olfactory coding and memory at multiple timescales

Insects can learn, allowing them great flexibility for locating seasonal food sources and avoiding wily predators. Because insects are relatively simple and accessible to manipulation, they provide good experimental preparations for exploring mechanisms underlying sensory coding and memory. Here we review how the intertwining of memory with computation enables the coding, decoding, and storage of sensory experience at various stages of the insect olfactory system. Individual parts of this system are capable of multiplexing memories at different timescales, and conversely, memory on a given timescale can be distributed across different parts of the circuit. Our sampling of the olfactory system emphasizes the diversity of memories, and the importance of understanding these memories in the context of computations performed by different parts of a sensory system.     

Elephants in space and time

Autocorrelation in animal movements can be both a serious nuisance to analysis and a source of valuable information about the scale and patterns of animal behavior, depending on the question and the techniques employed. In this paper we present an approach to analyzing the patterns of autocorrelation in animal movements that provides a detailed picture of seasonal variability in the scale and patterns of movement. We used a combination of moving window Mantel correlograms, surface correlation and crosscorrelation analysis to investigate the scales and patterns of autocorrelation in the movements of three herds of elephants in northern Botswana. Patterns of autocorrelation of elephant movements were long‐range, temporally complicated, seasonally variable, and closely linked with the onset of rainfall events. Specifically, for the three elephant herds monitored there was often significant autocorrelation among locations up to lags of 30 days or more. During many seasonal periods there was no indication of decreasing autocorrelation with increasing time between locations. Over the course of the year, herds showed highly variable and complex patterns of autocorrelation, ranging from random use of temporary home ranges, periodic use of focal areas, and directional migration. Even though the patterns of autocorrelation were variable in time and quite complex, there were highly significant correlations among the autocorrelation patterns of the different herds, indicating that they exhibited similar patterns of movement through the year. These major patterns of autocorrelation seem to be related to patterns of rainfall. The strength of correlation in movement patterns of the different herds decreased markedly at the cessation of major rain events. Also, there was a strong crosscorrelation between strength of autocorrelation of movement and rainfall, peaking at time lags of between three and four weeks. Overall, these approaches provide a powerful way to explore the scales and patterns of autocorrelation of animal movements, and to explicitly link those patterns to temporally variable environmental attributes, such as rainfall or vegetation phenology.     

Interhemispheric olfactory circuit and the memory beyond

In mammals, olfactory sensory neurons project their axons exclusively to the ipsilateral olfactory bulb. It remains unclear how odor information interacts between the two hemispheres of the brain. In this issue of Neuron, Yan et al. describe the precise interbulbar connection through the anterior olfactory nucleus pars externa (AONpE), which links contralateral isotypic olfactory columns.     

Tormogen cell and receptor-lymph space in insect olfactory sensilla

Summary (1) The basiconic sensilla on the antennae of Calliphora resemble other insect epidermal sensilla; one or several bipolar sense cells are surrounded by three non-neural cells. (2) The apical cell membrane of the tormogen cell(one of the three accessory cells) forms microvilli coated internally with particles. (3) In the (extracellular) outer receptor-lymph space hyaluronic acid can be demonstrated histochemically. (4) Demonstration of non-specific alkaline phosphatase, Mg²⁺-activated ATPase, and the presence of mitochondria in the apical part of the tormogen cell suggest active transport processes through these cells into the outer receptor-lymph space.Supported by the Deutsche Forschungsgemeinschaft     

NMDA receptors mediate olfactory learning and memory in Drosophila

BACKGROUND: Molecular and electrophysiological properties of NMDARs suggest that they may be the Hebbian "coincidence detectors" hypothesized to underlie associative learning. Because of the nonspecificity of drugs that modulate NMDAR function or the relatively chronic genetic manipulations of various NMDAR subunits from mammalian studies, conclusive evidence for such an acute role for NMDARs in adult behavioral plasticity, however, is lacking. Moreover, a role for NMDARs in memory consolidation remains controversial. RESULTS: The Drosophila genome encodes two NMDAR homologs, dNR1 and dNR2. When coexpressed in Xenopus oocytes or Drosophila S2 cells, dNR1 and dNR2 form functional NMDARs with several of the distinguishing molecular properties observed for vertebrate NMDARs, including voltage/Mg(2+)-dependent activation by glutamate. Both proteins are weakly expressed throughout the entire brain but show preferential expression in several neurons surrounding the dendritic region of the mushroom bodies. Hypomorphic mutations of the essential dNR1 gene disrupt olfactory learning, and this learning defect is rescued with wild-type transgenes. Importantly, we show that Pavlovian learning is disrupted in adults within 15 hr after transient induction of a dNR1 antisense RNA transgene. Extended training is sufficient to overcome this initial learning defect, but long-term memory (LTM) specifically is abolished under these training conditions. CONCLUSIONS: Our study uses a combination of molecular-genetic tools to (1) generate genomic mutations of the dNR1 gene, (2) rescue the accompanying learning deficit with a dNR1+ transgene, and (3) rapidly and transiently knockdown dNR1+ expression in adults, thereby demonstrating an evolutionarily conserved role for the acute involvement of NMDARs in associative learning and memory.     

Population variability in space and time

One of the most ubiquitous phenomena of all natural populations is their variability in numbers in space and time. However, there are notable differences among populations in the way the population size fluctuates. One of the major challenges in population and community ecology is to explain and understand this variety and to find possible underlying rules that might be modified from case-to-case. Population variability also has a spatial component because fluctuations are often synchronized over relatively large distances. Recently, this has led to growing interest in how 'internal' (density-dependent) processes interact with 'external' factors such as environmental variability.     

Niche dynamics in space and time

Niche conservatism, the tendency of a species niche to remain unchanged over time, is often assumed when discussing, explaining or predicting biogeographical patterns. Unfortunately, there has been no basis for predicting niche dynamics over relevant timescales, from tens to a few hundreds of years. The recent application of species distribution models (SDMs) and phylogenetic methods to analysis of niche characteristics has provided insight to niche dynamics. Niche shifts and conservatism have both occurred within the last 100 years, with recent speciation events, and deep within clades of species. There is increasing evidence that coordinated application of these methods can help to identify species which likely fulfill one key assumption in the predictive application of SDMs: an unchanging niche. This will improve confidence in SDM-based predictions of the impacts of climate change and species invasions on species distributions and biodiversity.     

Cell-signalling dynamics in time and space

The specificity of cellular responses to receptor stimulation is encoded by the spatial and temporal dynamics of downstream signalling networks. Temporal dynamics are coupled to spatial gradients of signalling activities, which guide pivotal intracellular processes and tightly regulate signal propagation across a cell. Computational models provide insights into the complex relationships between the stimuli and the cellular responses, and reveal the mechanisms that are responsible for signal amplification, noise reduction and generation of discontinuous bistable dynamics or oscillations.     

Experimental evolution of olfactory memory in Drosophila melanogaster

In order to address the nature of genetic variation in learning performance, we investigated the response to classical olfactory conditioning in "high-learning" Drosophila melanogaster lines previously subject to selection for the ability to learn an association between the flavor of an oviposition medium and bitter taste. In a T-maze choice test, the seven high-learning lines were better at avoiding an odor previously associated with aversive mechanical shock than were five unselected "low-learning" lines originating from the same natural population. Thus, the evolved improvement in learning ability of high-learning lines generalized to another aversion learning task involving a different aversive stimulus (shock instead of bitter taste) and a different behavioral context than that used to impose selection. In this olfactory shock task, the high-learning lines showed improvements in the learning rate as well as in two forms of consolidated memory: anesthesia-resistant memory and long-term memory. Thus, genetic variation underlying the experimental evolution of learning performance in the high-learning lines affected several phases of memory formation in the course of olfactory aversive learning. However, the two forms of consolidated memory were negatively correlated among replicate high-learning lines, which is consistent with a recent hypothesis that these two forms of consolidated memory are antagonistic.     

RNA logic in time and space

An EMBO-sponsored workshop entitled "Translational Control in Development and Neurobiology" was held recently in Mallorca, Spain. The talks covered mechanisms of translational regulation, particularly in terms of temporal and spatial regulation, over a wide range of biological systems.     

Associative learning and memory in Drosophila: beyond olfactory conditioning

The associative learning abilities of the fruit fly, Drosophila melanogaster, have been demonstrated in both classical and operant conditioning paradigms. Efforts to identify the neural pathways and cellular mechanisms of learning have focused largely on olfactory classical conditioning. Results derived from various genetic and molecular manipulations provide considerable evidence that this form of associative learning depends critically on neural activity and cAMP signaling in brain neuropil structures called mushroom bodies. Three other behavioral learning paradigms in Drosophila serve as the main subject of this review. These are (1) visual and motor learning of flies tethered in a flight simulator, (2) a form of spatial learning that is independent of visual and olfactory cues, and (3) experience-dependent changes in male courtship behavior. The present evidence suggests that at least some of these modes of learning are independent of mushroom bodies. Applying targeted genetic manipulations to these behavioral paradigms should allow for a more comprehensive understanding of neural mechanisms responsible for diverse forms of associative learning and memory.     

Higher olfactory processes: perceptual learning and memory.

The past year has seen several important findings emerge from studies of higher olfactory processes. The identification of synaptic long-term potentiation in the olfactory cortex, induced via repetitive burst stimulation at the theta rhythm, and physiological activity patterns associated with learning, some of which mimic long-term potentiation induction patterns, have suggested relationships between rhythmic activity, behavioral learning and synaptic plasticity. In addition, the construction of computational models of the olfactory bulb and cortex have generated testable behavioral and physiological predictions which have been supported by experimental evidence.     

Nuclear tumor suppressors in space and time

Numerous studies have identified key binding partners and functional activities of nuclear tumor-suppressor proteins such as the retinoblastoma protein, p53 and BRCA1. Historically, less attention has been given to the subnuclear locations of these proteins. Here, we describe several recent studies that promote the view that regulated association with subcompartments of the nucleus is inherent to tumor-suppressor function.     

The ediacaran biotas in space and time

The "Ediacaran organisms," which preceded and overlapped the Cambrian radiation of metazoans, include many fossils whose systematic positions remain contentious after over fifty years of study. It might seem that nothing particularly useful can be learned from a biota full of oddballs. However, analyses of the distribution of the Ediacaran organisms in time and space can be carried out without having to guess at the systematic position of the organisms. Combining these results with data on paleotectonics, paleoenvironmental parameters, and the ages of various assemblages sheds light on the origins, ecology, and even the systematic positions of the Ediacaran organisms. Parsimony Analysis of Endemism (PAE) confirms earlier studies in grouping Ediacaran biotas into three major clusters: the Avalon, White Sea, and Nama Assemblages. The available radiometric and stratigraphic data suggest that the Avalon is the oldest, the White Sea is next oldest, and the Nama extends to the base of the Cambrian. The "frondlike" Ediacaran taxa, and to a lesser extent the "medusoids," collectively show significantly longer stratigraphic ranges, broader geographical and paleoenvironmental ranges, and less provinciality than "bilaterian" and tubular taxa. Almost all tubular Ediacarans appear to be confined to equatorial areas, whereas other Ediacaran organisms show weak or no latitudinal diversity gradients. I conclude that the Ediacaran organisms show a diverse range of responses to various environmental parameters. There is no basis for classifying them all as having a single body plan and mode of life, as has often been done in the past.     

The spindle-assembly checkpoint in space and time

In eukaryotes, the spindle-assembly checkpoint (SAC) is a ubiquitous safety device that ensures the fidelity of chromosome segregation in mitosis. The SAC prevents chromosome mis-segregation and aneuploidy, and its dysfunction is implicated in tumorigenesis. Recent molecular analyses have begun to shed light on the complex interaction of the checkpoint proteins with kinetochores--structures that mediate the binding of spindle microtubules to chromosomes in mitosis. These studies are finally starting to reveal the mechanisms of checkpoint activation and silencing during mitotic progression.