Flight Activity Initiated via Giant Interneurons of the Cockroach: Evidence for Bifunctional Trigger Interneurons

Activity in dorsal giant interneurons of the cockroach initiates flight movements if leg contact with a substrate is prevented. The same interneurons initiate activity associated with running when leg contact is maintained. Thus, which one of two completely different behaviors the giant interneurons evoke depends on the presence or absence of leg contact.     

Extracellular potassium ions mediate specific neuronal interaction

The giant interneurons from the nerve system of the cockroach Periplaneta americana exhibit a peculiar reciprocal synaptic interaction. The synaptic potentials are not blocked by addition of 5 millimolar cobalt chloride and have an extrapolated reversal potential close to 0 millivolt. Hyperpolarizing current injected into one cell does not spread to the other. Intracellular injection of tetraethylammonium ions into one giant interneuron increases the duration of the action potential of the injected cell to 30 milliseconds and reduces the rise time and amplitude of the postsynaptic response recorded in the other giant interneuron. These results indicate that the interaction between the interneurons is not mediated by conventional chemical or electrotonic synapses.. All evidence points to generation of the potentials by localized increases in extracellular potassium concentrations as a consequence of firing of one neuron.     

Identified interneurons produce both primary afferent depolarization and presynaptic inhibition

Crayfish interneurons were identified that appear to be directly responsible for presynaptic inhibition of primary afferent synapses during crayfish escape behavior. The interneurons are fired by a polysynaptic pathway triggered by the giant escape command axons. When directly stimulated, these interneurons produce short-latency, chloride-dependent primary afferent depolarizations and presynaptically inhibit primary afferent input to mechanosensory interneurons.     

Reciprocal inhibition and postinhibitory rebound produce reverberation in a locomotor pattern generator

The central pattern generator for swimming in the pteropod mollusk Clione limacina consists of at least four pedal interneurons, two each controlling parapodial upstroke and downstroke. The two sets of antagonistic interneurons are linked by reciprocal monosynaptic inhibitory synapses, and all exhibit apparently strong postinhibitory rebound. This simple neuronal network produces reverberating alternate cyclic activity in the absence of tonic drive or apparent feedback modulation.     

Organizing principles for a diversity of GABAergic interneurons and synapses in the neocortex

A puzzling feature of the neocortex is the rich array of inhibitory interneurons. Multiple neuron recordings revealed numerous electrophysiological-anatomical subclasses of neocortical gamma-aminobutyric acid-ergic (GABAergic) interneurons and three types of GABAergic synapses. The type of synapse used by each interneuron to influence its neighbors follows three functional organizing principles. These principles suggest that inhibitory synapses could shape the impact of different interneurons according to their specific spatiotemporal patterns of activity and that GABAergic interneuron and synapse diversity may enable combinatorial inhibitory effects in the neocortex.     

Regeneration of functional synapses between individual recognizable neurons in the lamprey spinal cord

In 4- to 5-year-old sea lamprey larvae that had recovered from complete transection of the spinal cord, pairs of giant interneurons on opposite sides of the scar were impaled with microelectrodes. In 4 of 30 pairs, stimulation of the caudal cell elicited a monosynaptic electrochemical excitatory postsynaptic potential in the rostral cell. Fifty percent of such pairs were synaptically linked in control lampreys without transections. These results show regeneration of functional synaptic connections between individual neurons in a vertebrate central nervous system.     

Actin-based plasticity in dendritic spines

The central nervous system functions primarily to convert patterns of activity in sensory receptors into patterns of muscle activity that constitute appropriate behavior. At the anatomical level this requires two complementary processes: a set of genetically encoded rules for building the basic network of connections, and a mechanism for subsequently fine tuning these connections on the basis of experience. Identifying the locus and mechanism of these structural changes has long been among neurobiology's major objectives. Evidence has accumulated implicating a particular class of contacts, excitatory synapses made onto dendritic spines, as the sites where connective plasticity occurs. New developments in light microscopy allow changes in spine morphology to be directly visualized in living neurons and suggest that a common mechanism, based on dynamic actin filaments, is involved in both the formation of dendritic spines during development and their structural plasticity at mature synapses.     

Target cell-dependent normalization of transmitter release at neocortical synapses

The efficacy and short-term modification of neocortical synaptic connections vary with the type of target neuron. We investigated presynaptic Ca2+ and release probability at single synaptic contacts between pairs of neurons in layer 2/3 of the rat neocortex. The amplitude of Ca2+ signals in boutons of pyramids contacting bitufted or multipolar interneurons or other pyramids was dependent on the target cell type. Optical quantal analysis at single synaptic contacts suggested that release probabilities are also target cell-specific. Both the Ca2+ signal and the release probability of different boutons of a pyramid contacting the same target cell varied little. We propose that the mechanisms that regulate the functional properties of boutons of a pyramid normalize the presynaptic Ca2+ influx and release probability for all those boutons that innervate the same target cell.     

Newly identified 'glutamate interneurons' and their role in locomotion in the lamprey spinal cord

A new class of excitatory premotor interneurons that are important in the generation of locomotion in the lamprey has now been described. In the isolated spinal cord, these neurons act simultaneously with their postsynaptic motoneurons during fictive swimming. They are small and numerous, and they monosynaptically excite both motoneurons and inhibitory premotor interneurons. The excitatory postsynaptic potentials are depressed by an antagonist of excitatory amino acids. These interneurons receive reticulospinal input from the brain stem and polysynaptic input form skin afferents. A model of the network underlying locomotion based on the synaptic interactions of these neurons can now be proposed for the lamprey.     

Neuronal generation of the leech swimming movement

The swimming movement of the leech is produced by an ensemble of bilaterally symmetric, rhythmically active pairs of motor neurons present in each segmental ganglion of the ventral nerve cord. These motor neurons innervate the longitudinal muscles in dorsal or ventral sectors of the segmental body wall. Their duty cycles are phase-locked in a manner such that the dorsal and ventral body wall sectors of any given segment undergo an antiphasic contractile rhythm and that the contractile rhythms of different segments form a rostrocaudal phase progression. This activity rhythm is imposed on the motor neurons by a central swim oscillator, of which four bilaterally symmetric pairs of interneurons present in each segmental ganglion appear to constitute the major component. These interneurons are linked intra- and intersegmentally via inhibitory connections to form a segmentally iterated and inter-segmentally concatenated cyclic neuronal network. The network appears to owe its oscillatory activity pattern to the mechanism of recurrent cyclic inhibition.     

Permeability and structure of junctional membranes at an electrotonic synapse

The dye Procion Yellow M4RS crosses junctional membranes from cytoplasm to cytoplasm at electrotonic synapses between segments of the crayfish septate axon. The dye does not enter the cells from extracellular space. Thus permeability of junctional membranes is qualitatively different from that of nonjunctional membranes. Electron microscopy after fixation in the presence of lanthanum hydroxide indicates that these synapses are "gap junctions" and that there is a network of channels continuous with extracellular space between apposed junctional membranes. These channels must be interlaced with intercytoplasmic channels that are not open to extracellular space.     

Steroid-dependent survival of identifiable neurons in cultured ganglia of the moth Manduca sexta

Adult emergence at the end of metamorphosis in the moth Manduca sexta is followed by the death of abdominal interneurons and motoneurons. Abdominal ganglia removed from insects before this period of naturally occurring cell death and maintained in vitro showed neuronal death confined to the same cells that normally die in vivo. Addition of physiological levels of the steroid 20-hydroxyecdysone to the culture system prevented the selective death of these motoneurons.     

Giant interneurons mediating equilibrium reception in an insect

In the burrowing cockroach Arenivaga, two giant interneurons in each connective of the ventral nerve cord provide gravity orientation information. The interneurons receive input from plumb bob-like equilibrium receptors on the ventral surface of the cerci. Ouir results support the theory that the cerci of cockroaches are specialized equilibrium organs.     

Neuronal circuit mediating escape responses in crayfish

The neuronal circuit underlying rapid abdominal flexion in response to phasic tactile stimulation comprises identified afferents, interneurons of two orders, a decision unit, and several motor neurons. The circuit is organized hierarchically as a " cascade" in which electrical synapses predominate at higher levels. Behavioral habituation results from lability at chemical junctions early in the pathway.     

Gap junctions compensate for sublinear dendritic integration in an inhibitory network

Electrically coupled inhibitory interneurons dynamically control network excitability, yet little is known about how chemical and electrical synapses regulate their activity. Using two-photon glutamate uncaging and dendritic patch-clamp recordings, we found that the dendrites of cerebellar Golgi interneurons acted as passive cables. They conferred distance-dependent sublinear synaptic integration and weakened distal excitatory inputs. Gap junctions were present at a higher density on distal dendrites and contributed substantially to membrane conductance. Depolarization of one Golgi cell increased firing in its neighbors, and inclusion of dendritic gap junctions in interneuron network models enabled distal excitatory synapses to drive network activity more effectively. Our results suggest that dendritic gap junctions counteract sublinear dendritic integration by enabling excitatory synaptic charge to spread into the dendrites of neighboring inhibitory interneurons.     

Neural regeneration: delayed formation of central contacts by insect sensory cells

Correlated anatomical and electrophysiological results demonstrate that sensory neurons, which differentiate de novo within the epidermis of regenerate abdominal cerci of crickets, enter the terminal ganglion and form functional central connections even when regeneration of the cerci is delayed through the greater part of postembryonic development. Stimulation of regenerate cerci evokes activity in giant interneurons which is normal by several physiological criteria.     

High-probability uniquantal transmission at excitatory synapses in barrel cortex

The number of vesicles released at excitatory synapses and the number of release sites per synaptic connection are key determinants of information processing in the cortex, yet they remain uncertain. Here we show that the number of functional release sites and the number of anatomically identified synaptic contacts are equal at connections between spiny stellate and pyramidal cells in rat barrel cortex. Moreover, our results indicate that the amount of transmitter released per synaptic contact is independent of release probability and the intrinsic release probability is high. These properties suggest that connections between layer 4 and layer 2/3 are tuned for reliable transmission of spatially distributed, timing-based signals.     

Sorting of striatal and cortical interneurons regulated by semaphorin-neuropilin interactions

Most striatal and cortical interneurons arise from the basal telencephalon, later segregating to their respective targets. Here, we show that migrating cortical interneurons avoid entering the striatum because of a chemorepulsive signal composed at least in part of semaphorin 3A and semaphorin 3F. Migrating interneurons expressing neuropilins, receptors for semaphorins, are directed to the cortex; those lacking them go to the striatum. Loss of neuropilin function increases the number of interneurons that migrate into the striatum. These observations reveal a mechanism by which neuropilins mediate sorting of distinct neuronal populations into different brain structures, and provide evidence that, in addition to guiding axons, these receptors also control neuronal migration in the central nervous system.     

Decremental Conduction over "Giant" Afferent Processes in an Arthropod

Four "giant" mechanoreceptive cells form part of a stretch receptor organ at the base of the uropod in the sand crab, Emerita (Crustacea, Anomura). Injection of the fluorescent dye Procion Yellow revealed that these sensory cells are monopolar with somata located in the central nervous system. No such cells have previously been described in arthropods. These neurons are also unusual in that they do not generate propagated action potentials; rather, they mediate stretch reflexes by transmission of graded, decremental potentials.     

Synapses of horizontal cells in rabbit and cat retinas

Horizontal cells in the retinas of cats and rabbits are morphologically similar; in both species, two types can be distinguished in Golgistained material. Horizontal cells and their processes are readily recognized in electron micrographs, and many of the horizontal cell processes appear to make synaptic contacts with dendrites and somata of bipolar cells, and probably with other horizontal cells. The synapses of the horizontal cell appear similar to chemical synaptic contacts described throughout the nervous system. With the finding of synaptic contacts, it seems clear that retinal horizontal cells should be classified as neurons.