Molecular and cellular organization of insect chemosensory neurons

Animals use their chemosensory systems to detect and discriminate among chemical cues in the environment. Remarkable progress has recently been made in our knowledge of the molecular and cellular basis of chemosensory perception in insects, based largely on studies in Drosophila. This progress has been possible due to the identification of gene families for olfactory and gustatory receptors, the use of electro-physiological recording techniques on sensory neurons, the multitude of genetic manipulations that are available in this species, and insights from several insect model systems. Recent studies show that the superfamily of chemoreceptor proteins represent the essential elements in chemosensory coding, endowing chemosensory neurons with their abilities to respond to specific sets of odorants, tastants or pheromones. Investigating how insects detect chemicals in their environment can show us how receptor protein structures relate to ligand binding, how nervous systems process complex information, and how chemosensory systems and genes evolve.     

Retinotopic organization of small-field-target-detecting neurons in the insect visual system

BACKGROUND: Despite having tiny brains and relatively low-resolution compound eyes, many fly species frequently engage in precisely controlled aerobatic pursuits of conspecifics. Recent investigations into high-order processing in the fly visual system have revealed a class of neurons, coined small-target-motion detectors (STMDs), capable of responding robustly to target motion against the motion of background clutter. Despite limited spatial acuity in the insect eye, these neurons display exquisite sensitivity to small targets. RESULTS: We recorded intracellularly from morphologically identified columnar neurons in the lobula complex of the hoverfly Eristalis tenax. We show that these columnar neurons with exquisitely small receptive fields, like their large-field counterparts recently described from both male and female flies, have an extreme selectivity for the motion of small targets. In doing so, we provide the first physiological characterization of small-field neurons in female flies. These retinotopically organized columnar neurons include both direction-selective and nondirection-selective classes covering a large area of visual space. CONCLUSIONS: The retinotopic arrangement of lobula columnar neurons sensitive to the motion of small targets makes a strong case for these neurons as important precursors in the local processing of target motion. Furthermore, the continued response of STMDs with such small receptive fields to the motion of small targets in the presence of moving background clutter places further constraints on the potential mechanisms underlying their small-target tuning.     

The structural organization of the snail sensory systems]

In the paper are reviewed the author's data on the structure of peripheral nervous system of the body wall, gravitational organs--statocysts, eyes, and organs of distant chemoreception--ommatophors, or posterior head tentacles, of the snails Helix vulgaris and Helix pomatia. Localization in the CNS of central parts of the main sensory systems is shown and some structural characteristics of them are described. The data on the organization of the procerebrum which takes part in processing of information from the receptors of the head tentacles are presented. By some morphological features the procerebrum may be considered as one of the highest associative centers of the snails. The data under consideration were obtained by means of silver impregnation by Golgi, retro- and anterograde infusion of CoCl2, horseradish peroxidase and Lucifer yellow into the nerves, as well as by means of a number of other classical histological techniques.     

Differentiation of insect sensory neurons in the absence of their normal synaptic targets.

Sensory neurons in the antenna of the moth, Manduca sexta, arise and differentiate during the 18 days of metamorphosis from pupa to adult, sending axons to the brain. To assess the trophic dependence of developing antennal neurons on their targets, we studied antennae from surgically debrained animals. If the brain is removed 1 to 45 hr after pupal ecdysis (before and during the period when antennal neurons arise by cell divisions), adult development can be triggered by injection of β-ecdysone; if the brain is removed 50 to 60 hr after pupal ecdysis (before antennal axons contact the brain), metamorphosis proceeds spontaneously. Neurons proliferate normally and differentiate extensively in the antennae of debrained animals. They acquire a characteristic size and shape, elaborate axons and dendrites, migrate to appropriate positions in the sensilla, accumulate components of a neurotransmitter system (acetylcholine, choline acetyltransferase, and acetylcholinesterase), and generate electrical responses to olfactory and mechanical stimuli. Antennal sensory neurons thus differ from a variety of vertebrate neurons, which fail to mature when deprived of their synaptic targets.     

Ectopic trkA expression mediates a NGF survival response in NGF- independent sensory neurons but not in parasympathetic neurons

We have investigated the role of trkA, the tyrosine kinase NGF receptor, in mediating the survival response of embryonic neurons to NGF. Embryonic trigeminal mesencephalic (TMN) neurons, which normally survive in the presence of brain-derived neurotrophic factor (BDNF) but not NGF, become NGF-responsive when microinjected with an expression vector containing trkA cDNA. In contrast, microinjection of ciliary neurotrophic factor (CNTF)-dependent embryonic ciliary neurons with the same construct does not result in the acquisition of NGF responsiveness by these neurons despite de novo expression of trkA mRNA and protein. The failure of trkA to result in an NGF-promoted survival response in ciliary neurons is not due to absence of the low-affinity NGF receptor, p75, in these neurons. Quantitative RT/PCR and immunocytochemistry showed that TMN and ciliary neurons both express p75 mRNA and protein. These findings not only provide the first direct experimental demonstration of trkA mediating a physiological response in an appropriate cell type, namely NGF-promoted survival of embryonic neurons, but indicate that not all neurons are able to respond to a trkA-mediated signal transduction event.     

Drosophila sensory neurons require Dscam for dendritic self-avoidance and proper dendritic field organization

A neuron's dendrites typically do not cross one another. This intrinsic self-avoidance mechanism ensures unambiguous processing of sensory or synaptic inputs. Moreover, some neurons respect the territory of others of the same type, a phenomenon known as tiling. Different types of neurons, however, often have overlapping dendritic fields. We found that Down's syndrome Cell Adhesion Molecule (Dscam) is required for dendritic self-avoidance of all four classes of Drosophila dendritic arborization (da) neurons. However, neighboring mutant class IV da neurons still exhibited tiling, suggesting that self-avoidance and tiling differ in their recognition and repulsion mechanisms. Introducing 1 of the 38,016 Dscam isoforms to da neurons in Dscam mutants was sufficient to significantly restore self-avoidance. Remarkably, expression of a common Dscam isoform in da neurons of different classes prevented their dendrites from sharing the same territory, suggesting that coexistence of dendritic fields of different neuronal classes requires divergent expression of Dscam isoforms.     

Ectopic sensory neurons in mutant cockroaches compete with normal cells for central targets.

The cercus of the first instar cockroach, Periplaneta americana, bears two filiform hairs, lateral (L) and medial (M), each of which is innervated by a single sensory neuron. These project into the terminal ganglion of the CNS where they make synaptic connections with a number of ascending interneurons. We have discovered mutant animals that have more hairs on the cercus; the most typical phenotype, called "Space Invader" (SI), has an extra filiform hair in a proximo-lateral position on one of the cerci. The afferent neuron of this supernumerary hair (SIN) "invades the space" occupied by L in the CNS and makes similar synaptic connections to giant interneurons (GIs). SIN and L compete for these synaptic targets: the size of the L EPSP in a target interneuron GI3 is significantly reduced in the presence of SIN. Morphometric analysis of the L afferent in the presence or absence of SIN shows no anatomical concomitant of competition. Ablation of L afferent allows SIN to increase the size of its synaptic input to GI3. Less frequently in the mutant population, we find animals with a supernumerary medical (SuM) sensillum. Its afferent projects to the same neuropilar region as the M afferent, makes the same set of synaptic connections to GIs, and competes with M for these synaptic targets. The study of these competitive interactions between identified afferents and identified target interneurons reveals some of the dynamic processes that go on in normal development to shape the nervous system.     

Distribution of neurons responding to sensory stimuli and organization of topic projections in the cat caudate nucleus

The distribution of neurons responding to presentation of different sensory stimuli was investigated during chronic experiments on cats. These showed that cells responding to somatic and visual stimulation were unevenly distributed and that areas with differing levels of activity within the same nucleus alternated. No single topic projection was identified within the structure reaching the entire nucleus. The findings were compared with those found during morphological research indicating heterogeneity in caudate nucleus structure, implying the existence of neuronal groupings (or striosomes) belonging to a topically organized projection from the animal's body.Institute for Research into Information Transmission, Academy of Sciences of the USSR, Moscow. Translated from Neirofiziologiya, Vol. 22, No. 2, pp. 156–162, March–April, 1990.     

The organization of sensory cortex

Recent studies of primary visual cortex (V1) redefine layers 3 and 4 of V1 in monkeys and show that monkeys, apes and humans have different laminar specializations. Projections from V1 define a smaller, but complete, third visual area, and a dorsomedial area. The middle temporal visual area has two types of motion-sensitive modules with inputs from cytochrome oxidase columns in V1. Second-level somatosensory areas have been described in humans, and a second-level auditory area is shown to respond to somatosensory stimuli.     

Hierarchical organization of macaque and cat cortical sensory systems explored with a novel network processor

Neuroanatomists have described a large number of connections between the various structures of monkey and cat cortical sensory systems. Because of the complexity of the connection data, analysis is required to unravel what principles of organization they imply. To date, analysis of laminar origin and termination connection data to reveal hierarchical relationships between the cortical areas has been the most widely acknowledged approach. We programmed a network processor that searches for optimal hierarchical orderings of cortical areas given known hierarchical constraints and rules for their interpretation. For all cortical systems and all cost functions, the processor found a multitude of equally low-cost hierarchies. Laminar hierarchical constraints that are presently available in the anatomical literature were therefore insufficient to constrain a unique ordering for any of the sensory systems we analysed. Hierarchical orderings of the monkey visual system that have been widely reported, but which were derived by hand, were not among the optimal orderings. All the cortical systems we studied displayed a significant degree of hierarchical organization, and the anatomical constraints from the monkey visual and somato-motor systems were satisfied with very few constraint violations in the optimal hierarchies. The visual and somato-motor systems in that animal were therefore surprisingly strictly hierarchical. Most inconsistencies between the constraints and the hierarchical relationships in the optimal structures for the visual system were related to connections of area FST (fundus of superior temporal sulcus). We found that the hierarchical solutions could be further improved by assuming that FST consists of two areas, which differ in the nature of their projections. Indeed, we found that perfect hierarchical arrangements of the primate visual system, without any violation of anatomical constraints, could be obtained under two reasonable conditions, namely the subdivision of FST into two distinct areas, whose connectivity we predict, and the abolition of at least one of the less reliable rule constraints. Our analyses showed that the future collection of the same type of laminar constraints, or the inclusion of new hierarchical constraints from thalamocortical connections, will not resolve the problem of multiple optimal hierarchical representations for the primate visual system. Further data, however, may help to specify the relative ordering of some more areas. This indeterminacy of the visual hierarchy is in part due to the reported absence of some connections between cortical areas. These absences are consistent with limited cross-talk between differentiated processing streams in the system. Hence, hierarchical representation of the visual system is affected by, and must take into account, other organizational features, such as processing streams.     

Neuropeptides in sensory neurons

Substance P, somatostatin, VIP, CCK, angiotensin II, and bombesin have all been localized by immunohistochemical or radioimmunological means in neurons of sensory ganglia or in the dorsal horn of the spinal cord. Most of these neuropeptides have electrophysiological effects on spinal neurons and for substance P and somatostatin, these effects have been associated with particular sensory modalities. Newer investigations using the compound capsaicin are consistent with the hypothesis that substance P is an important neurochemical mediator of certain kinds of noxious peripheral stimuli. The newly described substance P antagonists promise to be important pharmacological tools for investigation of the long-neglected neurochemical bases of sensory neuron function. Elaboration of the roles of these sensory neuropeptides will no doubt shed light on many disease states in which there seems to be sensory neuron involvement.     

Central organization of the sensory function of the brain

Modern methodologies of the study of the brain sensory activity, basic data on the mechanisms of information coding and a number of hypotheses on information decoding are presented. A new concept of the sensory function of the brain united two main properties (coding and decoding) according to the dominant motivation and past experience is formulated.     

Functions of the LE sensory neurons inAplysia

Mechanosensory neurons which innervate the siphon and have their cell bodies in the LE cluster of the abdominal ganglion ofAplysia have revealed many cellular and molecular processes that may play general roles in learning and memory. It was initially suggested that these cells are largely responsible for triggering the gill-withdrawal reflex evoked by weak siphon stimulation, and that most of this effect is mediated by their monosynaptic connections to gill motor neurons. This implied a simple link between plasticity at these synapses and modifications of the reflex during learning. We review more recent studies from several laboratories showing that the LE cells are not activated by very weak tactile stimuli that elicit the gill-withdrawal reflex, and that an unidentified population of siphon sensory neurons has lower mechanosensory thresholds and produces shorter latency responses. Furthermore, the direct connections between LE cells and gill motor neurons make a minor contribution when the reflex is elicited in pinned siphon preparations by light stimuli that weakly activate the LE cells. Because weak mechanical stimulation of the unrestrained siphon causes little or no LE cell activation, it is unlikely that, under natural conditions, sensitization or conditioning of reflex responses elicited by light siphon touch depends upon plasticity of LE cell synapses onto either motor or interneurons. The LE cells appear to function as nociceptors because they are tuned to noxious stimuli and, like mammalian nociceptors, show peripheral sensitization following nociceptive activation. This sensitization and the profound activity-dependent potentiation of LE synapses indicate that LE cell contributions to defensive reflexes should be largest during and after intense activation of the LE cells by noxious stimulation (with the LE cell plasticity contributing to long-lasting memory of peripheral injury). The LE sensory neurons offer special opportunities for direct tests of this and other hypotheses about specific mnemonic functions of fundamental mechanisms of neural plasticity.     

Inflammation-mediated hyperexcitability of sensory neurons

One of the most prominent signs of tissue injury and inflammation is pain and pain continues to be the primary reason people seek medical attention. Inflammatory pain reflects, at least in part, an increase in the excitability, or sensitization, of subpopulations of primary afferent neurons. While the sensitization of high threshold afferents was observed almost 40 years ago, the basis for this phenomenon continues to be an active and fertile area of research today. This review will summarize recent advances in our mechanistic understanding of sensitization, focusing on four general areas where re search has been most active or productive. These include: (1) the characterization of second messenger pathways underlying inflammation-induced changes in afferent excitability; (2) the impact of previous injury on the afferent response to subsequent inflammation; (3) the impact of target of innervation on the specific afferent response to inflammation, and (4) the impact of sex hormones on the sensitization of high threshold afferents. Work in these areas highlights how much has been learned about this process as well as how much there is yet to learn.     

Spatial organization of antennal olfactory sensory neurons in the female Spodoptera littoralis moth: differences in sensitivity and temporal characteristics

Single-cell recordings from olfactory sensory neurons (OSNs), housed in sensilla located at the base and at the tip of the antenna, showed selective responses to plant odors and female sex pheromone in this polyphagous moth. A spatial variation existed in sensitivity: OSNs present on the more proximal segment (P) were more sensitive than those on the more distal segment (D). OSNs of the 2 locations also differed in temporal characteristics: OSNs on P had shorter latency and displayed more phasic responses, whereas those on D had more tonic responses, especially at low stimulus concentrations. The 196 OSNs responding to our 35 monomolecular stimuli in the screening were housed in 32 functional sensillum types: 27 in basiconic, 3 in long-trichoid, 2 in coeloconic, and 3 in auricillic sensilla. The OSNs in basiconic, coeloconic, and auricillic sensilla responded to plant-associated odorants, whereas OSNs in long-trichoid sensilla responded to female-produced sex pheromone components. Short-trichoid sensilla showed spontaneous activity, but no responses to any odorant tested. OSN specificity to plant stimuli ranged from highly specific to broadly tuned, but it did not differ clearly from females in more specialized moths. OSN response diversity is discussed in terms of olfactory coding, behavior, and ecological specialization.